diff --git a/.github/workflows/pr-craft-compose-integration.yml b/.github/workflows/pr-craft-compose-integration.yml
index 18b0c30eba..64bd5f183d 100644
--- a/.github/workflows/pr-craft-compose-integration.yml
+++ b/.github/workflows/pr-craft-compose-integration.yml
@@ -51,7 +51,7 @@ env:
   SANDBOX_CONTAINER_IMAGE: "onyxdotapp/sandbox:ci"
   # Read by api_server on boot; Sandbox containers call back via this URL on the
   # compose bridge.
-  SANDBOX_API_SERVER_URL: "http://api_server:8080"
+  ONYX_SERVER_URL: "http://api_server:8080"
 
 jobs:
   changes:
diff --git a/.github/workflows/pr-craft-k8s-tests.yml b/.github/workflows/pr-craft-k8s-tests.yml
index a13dda9c94..0aaa679c09 100644
--- a/.github/workflows/pr-craft-k8s-tests.yml
+++ b/.github/workflows/pr-craft-k8s-tests.yml
@@ -45,7 +45,7 @@ env:
   SANDBOX_SERVICE_ACCOUNT_NAME: "sandbox"
   SANDBOX_CONTAINER_IMAGE: "localhost:5001/onyx-sandbox:ci"
   # Sandbox pod resource requests live in values-ci.yaml (configMap.SANDBOX_POD_*).
-  SANDBOX_API_SERVER_URL: "http://onyx-api-service.onyx.svc.cluster.local:8080"
+  ONYX_SERVER_URL: "http://onyx-api-service.onyx.svc.cluster.local:8080"
 
   # Proxy lives in release namespace `onyx`. SANDBOX_PROXY_HOST is set
   # later to the proxy Service ClusterIP — the runner has no cluster DNS,
diff --git a/.vscode/.env.k8s.template b/.vscode/.env.k8s.template
index c46a751590..896452f9e5 100644
--- a/.vscode/.env.k8s.template
+++ b/.vscode/.env.k8s.template
@@ -140,7 +140,7 @@ SANDBOX_CONTAINER_IMAGE=onyxdotapp/sandbox:dev
 
 # How sandboxes reach the api_server: out through the egress proxy to the host
 # gateway, not internal cluster DNS. Linux-kind devs sub their own host gateway.
-SANDBOX_API_SERVER_URL=http://host.docker.internal:3000
+ONYX_SERVER_URL=http://host.docker.internal:3000/api
 
 SANDBOX_NAMESPACE=onyx-sandboxes
 
diff --git a/backend/onyx/sandbox_proxy/addons/gate.py b/backend/onyx/sandbox_proxy/addons/gate.py
index b1e0908be7..722f6b1b8b 100644
--- a/backend/onyx/sandbox_proxy/addons/gate.py
+++ b/backend/onyx/sandbox_proxy/addons/gate.py
@@ -60,7 +60,7 @@ from onyx.sandbox_proxy.logging_utils import (
 from onyx.sandbox_proxy.request_evaluator import RequestEvaluator
 from onyx.server.features.build.configs import (
     MCP_SESSION_TAG_HEADER,
-    SANDBOX_API_SERVER_URL,
+    ONYX_SERVER_URL,
     SANDBOX_APPROVAL_WAIT_TIMEOUT_SECONDS,
 )
 from onyx.server.features.build.db import action_approval
@@ -91,9 +91,9 @@ PARSER_MAX_BODY_BYTES = 32 * 1024 * 1024
 # in-cluster name resolving to an internal IP, while still denying every other port
 # on that host (e.g. a co-located Redis/Postgres reachable at the same hostname).
 def _parse_api_server() -> tuple[str | None, int | None]:
-    if not SANDBOX_API_SERVER_URL:
+    if not ONYX_SERVER_URL:
         return None, None
-    parsed = urlparse(SANDBOX_API_SERVER_URL)
+    parsed = urlparse(ONYX_SERVER_URL)
     host = (parsed.hostname or "").lower() or None
     port = parsed.port or (443 if parsed.scheme == "https" else 80)
     return host, port
diff --git a/backend/onyx/sandbox_proxy/resolvers/onyx_pat.py b/backend/onyx/sandbox_proxy/resolvers/onyx_pat.py
index 75c0aecd8b..e7b282f273 100644
--- a/backend/onyx/sandbox_proxy/resolvers/onyx_pat.py
+++ b/backend/onyx/sandbox_proxy/resolvers/onyx_pat.py
@@ -1,9 +1,9 @@
 """Onyx-API PAT credential resolver.
 
-Claims requests bound for the Onyx API host (the host of
-``SANDBOX_API_SERVER_URL``) and sets both auth headers to the sandbox's real
-per-sandbox PAT, read encrypted off ``Sandbox.encrypted_pat``. The tenant is
-embedded in the PAT itself, so no separate tenant header is injected.
+Claims requests bound for the Onyx API host (the host of ``ONYX_SERVER_URL``)
+and sets both auth headers to the sandbox's real per-sandbox PAT, read
+encrypted off ``Sandbox.encrypted_pat``. The tenant is embedded in the PAT
+itself, so no separate tenant header is injected.
 """
 
 from __future__ import annotations
@@ -24,7 +24,7 @@ from onyx.sandbox_proxy.credential_injection import (
     InjectionContext,
 )
 from onyx.sandbox_proxy.logging_utils import full_log_id, short_log_id
-from onyx.server.features.build.configs import SANDBOX_API_SERVER_URL
+from onyx.server.features.build.configs import ONYX_SERVER_URL
 from onyx.server.features.build.db.sandbox import get_sandbox_by_id
 from onyx.utils.logger import setup_logger
 
@@ -35,7 +35,7 @@ class OnyxPatResolver(CredentialResolver):
     """Injects the sandbox's Onyx API PAT on requests to the configured API host."""
 
     def __init__(self) -> None:
-        parsed = urlparse(SANDBOX_API_SERVER_URL) if SANDBOX_API_SERVER_URL else None
+        parsed = urlparse(ONYX_SERVER_URL) if ONYX_SERVER_URL else None
         host = parsed.hostname if parsed else None
         self._api_host = host.lower() if host else None
         if parsed is not None and host:
diff --git a/backend/onyx/server/features/build/configs.py b/backend/onyx/server/features/build/configs.py
index 585ac7d14a..938157815e 100644
--- a/backend/onyx/server/features/build/configs.py
+++ b/backend/onyx/server/features/build/configs.py
@@ -97,9 +97,9 @@ ENABLE_OPENCODE_DEBUGGING = (
     os.environ.get("ENABLE_OPENCODE_DEBUGGING", "false").lower() == "true"
 )
 
-# Must be set when SANDBOX_BACKEND=kubernetes (no default — varies per
-# deployment).
-SANDBOX_API_SERVER_URL = os.environ.get("SANDBOX_API_SERVER_URL", "")
+# Complete Onyx API base URL reachable from the sandbox, including any path
+# prefix. Must be set when SANDBOX_BACKEND=kubernetes.
+ONYX_SERVER_URL = os.environ.get("ONYX_SERVER_URL", "")
 
 # ==============================================================================
 # Sandbox egress proxy
diff --git a/backend/onyx/server/features/build/sandbox/README.md b/backend/onyx/server/features/build/sandbox/README.md
index e7f83088d5..b26eecb234 100644
--- a/backend/onyx/server/features/build/sandbox/README.md
+++ b/backend/onyx/server/features/build/sandbox/README.md
@@ -54,9 +54,13 @@ The Docker backend is intentionally the closest single-VM analogue of the Kubern
 
 #### Docker mode trust boundary
 
-`api_server` and `background` mount the host Docker socket so they can drive sandbox containers. Anything that can talk to that socket is effectively root on the host — only enable Craft on hosts you fully control. Sandbox containers themselves run unprivileged: `--security-opt no-new-privileges`, `--cap-drop ALL`, `user=1000:1000`, no Docker socket, and a fixed env allowlist (`ONYX_PAT` + `ONYX_SERVER_URL`).
+`api_server` and `background` mount the host Docker socket so they can drive sandbox containers. Anything that can talk to that socket is effectively root on the host — only enable Craft on hosts you fully control. Sandbox containers themselves run unprivileged: `--security-opt no-new-privileges`, `--cap-drop ALL`, `user=1000:1000`, no Docker socket, and a fixed env allowlist (`ONYX_PAT` + `ONYX_SERVER_URL` + `ONYX_API_PREFIX`).
 
-`SANDBOX_API_SERVER_URL` must be the **public** HTTPS URL that the agent reaches Onyx through (same way any onyx-cli client would). Compose hostnames like `http://api_server:8080` do not resolve from inside the sandbox bridge.
+`ONYX_SERVER_URL` is the complete API base URL used by both the host-side
+manager and the sandbox client. The Craft Compose overlay defaults it to
+`http://onyx-craft-api:8080`, a private alias on the sandbox bridge. Public
+reverse-proxy overrides must include their API path prefix, for example
+`https://onyx.your-org.example/api`.
 
 On EC2 the Docker bridge by default routes to `169.254.169.254` (IMDS), which can hand out IAM credentials. `install.sh --include-craft` installs a host-level `DOCKER-USER` iptables rule to drop sandbox→IMDS traffic when it has sudo/iptables access, and prints the manual command otherwise. There is no application-level fallback — fix this at the host firewall.
 
@@ -169,10 +173,10 @@ SANDBOX_SERVICE_ACCOUNT_NAME=sandbox      # No storage credentials required
 
 ```bash
 
-# Public URL the sandbox agent uses to reach Onyx (HTTPS, externally resolvable —
-# compose hostnames like http://api_server:8080 will not resolve from inside the
-# sandbox bridge).
-SANDBOX_API_SERVER_URL=https://onyx.your-org.example
+# Complete API base URL. The Craft Compose overlay defaults to its private
+# http://onyx-craft-api:8080 alias; override only to route through a public
+# reverse proxy.
+ONYX_SERVER_URL=https://onyx.your-org.example/api
 
 # Host path of the Docker socket mounted into api_server/background
 SANDBOX_DOCKER_SOCKET=/var/run/docker.sock      # Default: /var/run/docker.sock
@@ -222,7 +226,8 @@ uv run pytest backend/tests/integration/tests/craft/k8s/test_kubernetes_sandbox.
 - Confirm `api_server` actually has the Docker socket: `docker compose exec api_server ls -l /var/run/docker.sock`
 - Confirm the dedicated bridge exists: `docker network inspect onyx_craft_sandbox` (created by `install.sh --include-craft`, or run `docker network create onyx_craft_sandbox` manually)
 - Check sandbox logs: `docker logs sandbox-<id8>`
-- Confirm `SANDBOX_API_SERVER_URL` is a publicly resolvable HTTPS URL (the agent cannot reach `http://api_server:8080` from inside the sandbox bridge)
+- Confirm `ONYX_SERVER_URL` resolves from the sandbox bridge and includes any
+  API path prefix. The Compose default is `http://onyx-craft-api:8080`.
 
 ### Sandbox Stuck in PROVISIONING (Kubernetes)
 
@@ -252,7 +257,7 @@ uv run pytest backend/tests/integration/tests/craft/k8s/test_kubernetes_sandbox.
 - **Sandbox app containers and sidecar init containers** do not receive FileStore, S3, or MinIO credentials
 - **Network policies** can restrict sandbox egress traffic
 - **Resource limits** prevent resource exhaustion
-- **Docker containers** run with `--security-opt no-new-privileges`, `--cap-drop ALL`, `user=1000:1000`, no Docker socket, and a fixed env allowlist (`ONYX_PAT` + `ONYX_SERVER_URL`)
+- **Docker containers** run with `--security-opt no-new-privileges`, `--cap-drop ALL`, `user=1000:1000`, no Docker socket, and a fixed env allowlist (`ONYX_PAT` + `ONYX_SERVER_URL` + `ONYX_API_PREFIX`)
 - **Docker network isolation** is enforced by joining only the dedicated `onyx_craft_sandbox` bridge — compose's default network (postgres/redis/minio/model servers) is unreachable by DNS from inside a sandbox
 - **EC2 IMDS** must be blocked at the host firewall (`install.sh --include-craft` installs a `DOCKER-USER` iptables rule on EC2 when sudo is available) — there is no app-level fallback
 
diff --git a/backend/onyx/server/features/build/sandbox/docker/docker_sandbox_manager.py b/backend/onyx/server/features/build/sandbox/docker/docker_sandbox_manager.py
index 0f344dee80..75be357c59 100644
--- a/backend/onyx/server/features/build/sandbox/docker/docker_sandbox_manager.py
+++ b/backend/onyx/server/features/build/sandbox/docker/docker_sandbox_manager.py
@@ -29,6 +29,7 @@ Sandbox containers run with:
 - no Docker socket mount
 - no S3 / MinIO / Postgres / Redis / FileStore credentials in env
 - a fixed env allowlist (``ONYX_PAT``, ``ONYX_SERVER_URL``,
+  ``ONYX_API_PREFIX``,
   opencode auth/config only)
 - only the dedicated sandbox bridge network — never compose's default
   network. As a result api_server / postgres / redis / minio /
@@ -47,8 +48,9 @@ Outbound communication is intentionally limited to:
 1. Public internet over HTTPS (the bridge has default internet egress; block at
    the host's ``DOCKER-USER`` chain if you need a stricter posture, e.g. for EC2
    IMDS).
-2. The Onyx API via ``ONYX_SERVER_URL`` — which must be the *public* HTTPS URL
-   the agent reaches just like any other onyx-cli client.
+2. The Onyx API via the complete ``ONYX_SERVER_URL`` API base. The Craft
+   overlay uses a private alias on the sandbox bridge by default; deployments
+   may instead provide a public HTTPS API URL.
 
 Most control-plane traffic from api_server → sandbox uses the Docker
 Engine API (``docker exec``). Prompt/event transport uses opencode-serve over
@@ -82,10 +84,10 @@ from onyx.db.enums import SandboxStatus
 from onyx.file_store.file_store import get_default_file_store
 from onyx.server.features.build.configs import (
     ATTACHMENTS_DIRECTORY,
+    ONYX_SERVER_URL,
     OPENCODE_DISABLED_TOOLS,
     OPENCODE_SERVE_PORT,
     OPENCODE_SERVER_PASSWORD,
-    SANDBOX_API_SERVER_URL,
     SANDBOX_CONTAINER_IMAGE,
     SANDBOX_DOCKER_CPU_LIMIT,
     SANDBOX_DOCKER_MEMORY_LIMIT,
@@ -326,9 +328,9 @@ _COMPOSE_INTERNAL_HOSTNAMES = {
 def _looks_like_internal_compose_host(url: str) -> bool:
     """Heuristic: Does ``url`` reference a compose-internal service hostname?
 
-    Used to warn deployers that pointed SANDBOX_API_SERVER_URL at the
-    api_server's compose DNS name. Sandboxes can't resolve that — they only join
-    the craft bridge network — so the URL must be the public Onyx URL.
+    Used to warn deployers that pointed ONYX_SERVER_URL at a service available
+    only on Compose's default network. Sandboxes can resolve the dedicated
+    ``onyx-craft-api`` alias, but not these unrelated service names.
     """
     if not url:
         return False
@@ -542,10 +544,10 @@ def build_container_create_kwargs(
       ``firewall-init.sh`` to read ``ca.crt``. That volume also contains
       root-only ``ca.key``; the agent runs as UID 1000 after init.
 
-    ``ONYX_SERVER_URL`` must be the *public* Onyx URL (the one onyx-cli inside
-    the sandbox will hit over HTTPS) — not an internal compose DNS name. We emit
-    a warning if it looks like the latter, since reaching it would require the
-    sandbox to be on the compose default network.
+    ``ONYX_SERVER_URL`` is the complete API base used by onyx-cli inside the
+    sandbox. The default ``onyx-craft-api`` alias is attached to the sandbox
+    bridge; we warn about other Compose DNS names because they exist only on the
+    default network.
 
     ``opencode_password`` is generated per-provision by the manager and injected
     as the env var named by ``OPENCODE_SERVER_PASSWORD``. The api_server reads
@@ -556,16 +558,19 @@ def build_container_create_kwargs(
     """
     if _looks_like_internal_compose_host(api_server_url):
         logger.warning(
-            "SANDBOX_API_SERVER_URL=%s looks like an internal compose hostname. Sandboxes only "
-            "join the craft bridge network and reach the API server like any other public client, "
-            "so this URL must resolve publicly (e.g. https://onyx.your-org.com). Internal DNS will "
-            "fail and the agent will see 'connection refused'.",
+            "ONYX_SERVER_URL=%s looks like an internal compose hostname. Sandboxes only "
+            "join the craft bridge network, so default-network DNS will fail. Use the "
+            "http://onyx-craft-api:8080 bridge alias or a public API base such as "
+            "https://onyx.your-org.com/api.",
             api_server_url,
         )
 
     env: dict[str, str] = {
         "ONYX_PAT": onyx_pat,
         "ONYX_SERVER_URL": api_server_url,
+        # The deployment URL is already the exact API base. Disable the CLI's
+        # compatibility prefix for direct services and prefixed ingress URLs.
+        "ONYX_API_PREFIX": "",
         OPENCODE_SERVER_PASSWORD: opencode_password,
         "OPENCODE_CONFIG_CONTENT": opencode_config_json,
     }
@@ -832,11 +837,11 @@ class DockerSandboxManager(SandboxManager):
     ) -> SandboxInfo:
         if not onyx_pat:
             raise ValueError("onyx_pat is required for Docker sandbox provisioning.")
-        if not SANDBOX_API_SERVER_URL:
+        if not ONYX_SERVER_URL:
             raise ValueError(
-                "SANDBOX_API_SERVER_URL must be set for Docker sandbox provisioning."
+                "ONYX_SERVER_URL must be set for Docker sandbox provisioning."
             )
-        validate_sandbox_api_url(SANDBOX_API_SERVER_URL)
+        validate_sandbox_api_url(ONYX_SERVER_URL)
 
         logger.info(
             "Provisioning Docker sandbox %s for user %s, tenant %s.",
@@ -999,7 +1004,7 @@ class DockerSandboxManager(SandboxManager):
             tenant_id=tenant_id,
             image=self._image,
             onyx_pat=onyx_pat,
-            api_server_url=SANDBOX_API_SERVER_URL,
+            api_server_url=ONYX_SERVER_URL,
             network=self._network_name,
             volume_name=volume_name,
             memory_limit=self._memory_limit,
diff --git a/backend/onyx/server/features/build/sandbox/kubernetes/kubernetes_sandbox_manager.py b/backend/onyx/server/features/build/sandbox/kubernetes/kubernetes_sandbox_manager.py
index ccb5371c9e..d62fb872e3 100644
--- a/backend/onyx/server/features/build/sandbox/kubernetes/kubernetes_sandbox_manager.py
+++ b/backend/onyx/server/features/build/sandbox/kubernetes/kubernetes_sandbox_manager.py
@@ -64,10 +64,10 @@ from onyx.cache.interface import CACHE_TRANSIENT_ERRORS
 from onyx.db.enums import SandboxStatus
 from onyx.file_store.file_store import get_default_file_store
 from onyx.server.features.build.configs import (
+    ONYX_SERVER_URL,
     OPENCODE_DISABLED_TOOLS,
     OPENCODE_SERVE_PORT,
     OPENCODE_SERVER_PASSWORD,
-    SANDBOX_API_SERVER_URL,
     SANDBOX_CONTAINER_IMAGE,
     SANDBOX_NAMESPACE,
     SANDBOX_NEXTJS_PORT_END,
@@ -1048,11 +1048,11 @@ class KubernetesSandboxManager(SandboxManager):
 
         if not onyx_pat:
             raise ValueError("onyx_pat is required for Kubernetes sandbox provisioning")
-        if not SANDBOX_API_SERVER_URL:
+        if not ONYX_SERVER_URL:
             raise ValueError(
-                "SANDBOX_API_SERVER_URL must be set for Kubernetes sandbox provisioning"
+                "ONYX_SERVER_URL must be set for Kubernetes sandbox provisioning"
             )
-        validate_sandbox_api_url(SANDBOX_API_SERVER_URL)
+        validate_sandbox_api_url(ONYX_SERVER_URL)
         if not SANDBOX_PROXY_HOST:
             raise ValueError(
                 "SANDBOX_PROXY_HOST must be set for Kubernetes sandbox provisioning"
diff --git a/backend/onyx/server/features/build/sandbox/util/api_url_check.py b/backend/onyx/server/features/build/sandbox/util/api_url_check.py
index c5302c7ac8..81da394b74 100644
--- a/backend/onyx/server/features/build/sandbox/util/api_url_check.py
+++ b/backend/onyx/server/features/build/sandbox/util/api_url_check.py
@@ -1,10 +1,10 @@
-"""Provision-time validation of SANDBOX_API_SERVER_URL.
+"""Provision-time validation of ONYX_SERVER_URL.
 
-SANDBOX_API_SERVER_URL is the full base URL a sandbox client uses, any API
-path prefix included. The classic misconfiguration is a public URL without
-its /api prefix, which fails far from the cause: every LLM-gateway and
-onyx-cli call inside the sandbox 404s. Probe once per process at provision
-time and fail with the corrected value instead.
+ONYX_SERVER_URL is the full base URL a client uses, any API path prefix
+included. The classic misconfiguration is a public URL without its /api
+prefix, which fails far from the cause: every LLM-gateway and onyx-cli call
+inside the sandbox 404s. Probe once per process at provision time and fail
+with the corrected value instead.
 """
 
 import threading
@@ -68,7 +68,7 @@ def validate_sandbox_api_url(api_server_url: str) -> None:
     response = _probe_health(base)
     if response is None:
         logger.warning(
-            "Could not probe %s/health to validate SANDBOX_API_SERVER_URL; "
+            "Could not probe %s/health to validate ONYX_SERVER_URL; "
             "skipping the prefix check",
             base,
         )
@@ -91,14 +91,14 @@ def validate_sandbox_api_url(api_server_url: str) -> None:
     if prefixed_response is not None and _is_health_response(prefixed_response):
         raise OnyxError(
             OnyxErrorCode.INTERNAL_ERROR,
-            f"SANDBOX_API_SERVER_URL={api_server_url!r} is missing its API path "
+            f"ONYX_SERVER_URL={api_server_url!r} is missing its API path "
             f"prefix: {base}/health does not serve the API health payload "
             f"(HTTP {response.status_code}) while {prefixed}/health does. "
-            f"Set SANDBOX_API_SERVER_URL to {prefixed!r} — the full base URL a "
+            f"Set ONYX_SERVER_URL to {prefixed!r} — the full base URL a "
             "sandbox client uses.",
         )
     logger.warning(
-        "SANDBOX_API_SERVER_URL=%s: %s/health did not serve the API health "
+        "ONYX_SERVER_URL=%s: %s/health did not serve the API health "
         "payload (HTTP %s) and %s/health did not either; sandbox API calls "
         "will likely fail. Verify the URL is the full base URL including any "
         "path prefix.",
diff --git a/backend/tests/external_dependency_unit/craft/test_provisioning_lock.py b/backend/tests/external_dependency_unit/craft/test_provisioning_lock.py
index 148f7ba5a2..516084189a 100644
--- a/backend/tests/external_dependency_unit/craft/test_provisioning_lock.py
+++ b/backend/tests/external_dependency_unit/craft/test_provisioning_lock.py
@@ -133,7 +133,7 @@ def lock_env(
     preconditions (URL/proxy host) satisfied."""
     monkeypatch.setattr(factory, "CACHE_BACKEND", CacheBackendType.REDIS)
     monkeypatch.setattr(
-        kubernetes_sandbox_manager, "SANDBOX_API_SERVER_URL", "http://api-server"
+        kubernetes_sandbox_manager, "ONYX_SERVER_URL", "http://api-server"
     )
     monkeypatch.setattr(
         kubernetes_sandbox_manager, "SANDBOX_PROXY_HOST", "sandbox-proxy"
diff --git a/backend/tests/external_dependency_unit/sandbox_proxy/test_onyx_pat_resolver.py b/backend/tests/external_dependency_unit/sandbox_proxy/test_onyx_pat_resolver.py
index 3e9c670070..88e75a68e5 100644
--- a/backend/tests/external_dependency_unit/sandbox_proxy/test_onyx_pat_resolver.py
+++ b/backend/tests/external_dependency_unit/sandbox_proxy/test_onyx_pat_resolver.py
@@ -49,7 +49,7 @@ def test_claims_then_resolve_round_trips_minted_pat(
         matched_actions=None,
     )
 
-    monkeypatch.setattr(onyx_pat_mod, "SANDBOX_API_SERVER_URL", f"https://{_API_HOST}")
+    monkeypatch.setattr(onyx_pat_mod, "ONYX_SERVER_URL", f"https://{_API_HOST}")
     resolver = OnyxPatResolver()
     assert resolver.claims(MagicMock(host=_API_HOST, port=443), ctx) is True
     assert resolver.claims(MagicMock(host="slack.com", port=443), ctx) is False
diff --git a/backend/tests/unit/build/test_opencode_serve_ready_password_reset.py b/backend/tests/unit/build/test_opencode_serve_ready_password_reset.py
index 43d82f464a..5c1e51431a 100644
--- a/backend/tests/unit/build/test_opencode_serve_ready_password_reset.py
+++ b/backend/tests/unit/build/test_opencode_serve_ready_password_reset.py
@@ -101,7 +101,7 @@ def test_reuse_existing_pod_clears_stale_tombstone() -> None:
     mgr._terminated_sandboxes.add(sandbox_id)
 
     with (
-        mock.patch.object(k8s_mod, "SANDBOX_API_SERVER_URL", "http://api"),
+        mock.patch.object(k8s_mod, "ONYX_SERVER_URL", "http://api"),
         mock.patch.object(k8s_mod, "SANDBOX_PROXY_HOST", "proxy.local"),
         mock.patch.object(mgr, "_pod_exists_and_healthy", return_value=True),
         mock.patch.object(mgr, "_ensure_service_exists"),
diff --git a/backend/tests/unit/onyx/server/features/build/sandbox/test_docker_manager_config.py b/backend/tests/unit/onyx/server/features/build/sandbox/test_docker_manager_config.py
index 2f4301bc98..aaf402c711 100644
--- a/backend/tests/unit/onyx/server/features/build/sandbox/test_docker_manager_config.py
+++ b/backend/tests/unit/onyx/server/features/build/sandbox/test_docker_manager_config.py
@@ -250,7 +250,7 @@ def proxy_kwargs() -> ContainerCreateKwargs:
         tenant_id=TENANT_ID,
         image="onyxdotapp/sandbox:test",
         onyx_pat=SANDBOX_PROXY_INJECTED_PLACEHOLDER,
-        api_server_url="https://onyx.example.com",
+        api_server_url="https://onyx.example.com/api",
         network="onyx_craft_sandbox",
         volume_name="onyx-craft-sandbox-12345678",
         memory_limit="2g",
@@ -359,6 +359,7 @@ def test_container_kwargs_env_allowlist_excludes_storage_credentials(
     # Required env
     assert env["ONYX_PAT"] == "pat-redacted"
     assert env["ONYX_SERVER_URL"] == "http://api_server:8080"
+    assert env["ONYX_API_PREFIX"] == ""
     # opencode-serve transport wiring
     assert env["OPENCODE_SERVER_PASSWORD"] == _OPENCODE_PASSWORD
     assert env["OPENCODE_CONFIG_CONTENT"] == _OPENCODE_CONFIG_JSON
@@ -493,6 +494,7 @@ def test_container_kwargs_env_is_a_minimal_allowlist(
     assert set(env.keys()) == {
         "ONYX_PAT",
         "ONYX_SERVER_URL",
+        "ONYX_API_PREFIX",
         "OPENCODE_SERVER_PASSWORD",
         "OPENCODE_CONFIG_CONTENT",
     }
@@ -526,7 +528,7 @@ def test_container_kwargs_mounts_tmp_as_tmpfs(
 def test_container_kwargs_warns_on_internal_compose_host(
     caplog: pytest.LogCaptureFixture,
 ) -> None:
-    """Deployers that point SANDBOX_API_SERVER_URL at compose DNS get warned."""
+    """Deployers that point ONYX_SERVER_URL at compose DNS get warned."""
     import logging
 
     with caplog.at_level(logging.WARNING):
@@ -563,7 +565,7 @@ def test_container_kwargs_no_warning_for_public_url(
             tenant_id=TENANT_ID,
             image="onyxdotapp/sandbox:test",
             onyx_pat="pat",
-            api_server_url="https://onyx.example.com",
+            api_server_url="https://onyx.example.com/api",
             network="onyx_craft_sandbox",
             volume_name="vol",
             memory_limit="2g",
@@ -656,10 +658,11 @@ def test_proxy_kwargs_env_contains_proxy_and_ca_keys(
     contract vars.
     """
     env = proxy_kwargs["environment"]
-    # The legacy 4-key core is preserved; ONYX_PAT is the proxy placeholder in
-    # this posture (real value lives in Postgres, proxy injects on wire).
+    # The compatibility core is preserved; ONYX_PAT is the proxy placeholder
+    # in this posture (real value lives in Postgres, proxy injects on wire).
     assert env["ONYX_PAT"] == SANDBOX_PROXY_INJECTED_PLACEHOLDER
-    assert env["ONYX_SERVER_URL"] == "https://onyx.example.com"
+    assert env["ONYX_SERVER_URL"] == "https://onyx.example.com/api"
+    assert env["ONYX_API_PREFIX"] == ""
     assert env["OPENCODE_SERVER_PASSWORD"] == _OPENCODE_PASSWORD
     assert env["OPENCODE_CONFIG_CONTENT"] == _OPENCODE_CONFIG_JSON
     # firewall-init.sh contract.
@@ -729,6 +732,7 @@ def test_proxy_kwargs_env_is_a_locked_allowlist(
         # Legacy core
         "ONYX_PAT",
         "ONYX_SERVER_URL",
+        "ONYX_API_PREFIX",
         "OPENCODE_SERVER_PASSWORD",
         "OPENCODE_CONFIG_CONTENT",
         # firewall-init.sh contract
@@ -777,7 +781,7 @@ def test_proxy_kwargs_requires_ca_volume() -> None:
             tenant_id=TENANT_ID,
             image="onyxdotapp/sandbox:test",
             onyx_pat="pat",
-            api_server_url="https://onyx.example.com",
+            api_server_url="https://onyx.example.com/api",
             network="onyx_craft_sandbox",
             volume_name="vol",
             memory_limit="2g",
diff --git a/backend/tests/unit/onyx/server/features/build/sandbox/test_docker_serve_plumbing.py b/backend/tests/unit/onyx/server/features/build/sandbox/test_docker_serve_plumbing.py
index 772d3375c0..012019d1e5 100644
--- a/backend/tests/unit/onyx/server/features/build/sandbox/test_docker_serve_plumbing.py
+++ b/backend/tests/unit/onyx/server/features/build/sandbox/test_docker_serve_plumbing.py
@@ -46,6 +46,8 @@ def _bare_manager() -> DockerSandboxManager:
     mgr._agent_instructions_template_path = (  # type: ignore[attr-defined]
         dsm.Path(dsm.__file__).parent.parent.parent / "AGENTS.template.md"
     )
+    mgr._image_checked = False  # type: ignore[attr-defined]
+    mgr._image_check_lock = dsm.threading.Lock()  # type: ignore[attr-defined]
     mgr._init_serve_state()
     return mgr
 
@@ -316,7 +318,7 @@ def test_provision_generates_fresh_password_and_injects_into_container_env(
     every later request 401s.
     """
     monkeypatch.setattr(dsm, "DEV_MODE", True)
-    monkeypatch.setattr(dsm, "SANDBOX_API_SERVER_URL", "https://onyx.example.com")
+    monkeypatch.setattr(dsm, "ONYX_SERVER_URL", "https://onyx.example.com/api")
     monkeypatch.setattr(dsm, "validate_sandbox_api_url", lambda *_: None)
     # Skip the actual readiness HTTP probe — that needs a real container.
     monkeypatch.setattr(
@@ -376,6 +378,7 @@ def test_provision_generates_fresh_password_and_injects_into_container_env(
     assert set(env.keys()) == {
         "ONYX_PAT",
         "ONYX_SERVER_URL",
+        "ONYX_API_PREFIX",
         OPENCODE_SERVER_PASSWORD,
         "OPENCODE_CONFIG_CONTENT",
     }
@@ -475,7 +478,7 @@ def test_provision_removes_container_when_history_restore_fails(
     home.
     """
     monkeypatch.setattr(dsm, "DEV_MODE", True)
-    monkeypatch.setattr(dsm, "SANDBOX_API_SERVER_URL", "https://onyx.example.com")
+    monkeypatch.setattr(dsm, "ONYX_SERVER_URL", "https://onyx.example.com/api")
     monkeypatch.setattr(dsm, "validate_sandbox_api_url", lambda *_: None)
 
     mgr = _bare_manager()
diff --git a/backend/tests/unit/onyx/server/features/build/sandbox/test_k8s_push_error_mapping.py b/backend/tests/unit/onyx/server/features/build/sandbox/test_k8s_push_error_mapping.py
index e0c56ce947..5632b19220 100644
--- a/backend/tests/unit/onyx/server/features/build/sandbox/test_k8s_push_error_mapping.py
+++ b/backend/tests/unit/onyx/server/features/build/sandbox/test_k8s_push_error_mapping.py
@@ -41,6 +41,7 @@ from onyx.server.features.build.sandbox.image.sandbox_daemon.contract import (
 )
 from onyx.server.features.build.sandbox.kubernetes import sidecar_client
 from onyx.server.features.build.sandbox.kubernetes.kubernetes_sandbox_manager import (
+    OPENCODE_HISTORY_RESTORE_TIMEOUT_SECONDS,
     KubernetesSandboxManager,
     _build_targz,
 )
@@ -703,7 +704,7 @@ def test_restore_opencode_history_posts_archive_to_sidecar(
         assert archive_file.read() == archive_body
         assert sha256_hex == hashlib.sha256(archive_body).hexdigest()
         assert operation_label == "opencode history restore"
-        assert timeout_seconds == 300.0
+        assert timeout_seconds == OPENCODE_HISTORY_RESTORE_TIMEOUT_SECONDS
         calls.append("restore")
 
     sidecar_client = MagicMock()
@@ -737,7 +738,7 @@ def test_restore_opencode_history_marks_sidecar_ready_when_no_snapshot(
         assert sandbox_id == expected_sandbox_id
         assert endpoint_path == SIDECAR_OPENCODE_HISTORY_MARK_RESTORED_PATH
         assert operation_label == "opencode history restore marker"
-        assert timeout_seconds == 300.0
+        assert timeout_seconds == OPENCODE_HISTORY_RESTORE_TIMEOUT_SECONDS
 
     sidecar_client = MagicMock()
     sidecar_client.post_empty.side_effect = fake_mark_restored
@@ -753,7 +754,7 @@ def test_provision_cleans_up_pod_when_opencode_history_restore_fails(
 ) -> None:
     import onyx.server.features.build.sandbox.kubernetes.kubernetes_sandbox_manager as ksm
 
-    monkeypatch.setattr(ksm, "SANDBOX_API_SERVER_URL", "http://api-server")
+    monkeypatch.setattr(ksm, "ONYX_SERVER_URL", "http://api-server")
     monkeypatch.setattr(ksm, "validate_sandbox_api_url", lambda *_: None)
     monkeypatch.setattr(ksm, "SANDBOX_PROXY_HOST", "proxy.local")
 
@@ -798,7 +799,7 @@ def test_provision_existing_healthy_pod_does_not_restore_opencode_history(
 ) -> None:
     import onyx.server.features.build.sandbox.kubernetes.kubernetes_sandbox_manager as ksm
 
-    monkeypatch.setattr(ksm, "SANDBOX_API_SERVER_URL", "http://api-server")
+    monkeypatch.setattr(ksm, "ONYX_SERVER_URL", "http://api-server")
     monkeypatch.setattr(ksm, "validate_sandbox_api_url", lambda *_: None)
     monkeypatch.setattr(ksm, "SANDBOX_PROXY_HOST", "proxy.local")
 
@@ -836,7 +837,7 @@ def test_provision_conflicting_healthy_pod_skips_startup_restore(
 ) -> None:
     import onyx.server.features.build.sandbox.kubernetes.kubernetes_sandbox_manager as ksm
 
-    monkeypatch.setattr(ksm, "SANDBOX_API_SERVER_URL", "http://api-server")
+    monkeypatch.setattr(ksm, "ONYX_SERVER_URL", "http://api-server")
     monkeypatch.setattr(ksm, "validate_sandbox_api_url", lambda *_: None)
     monkeypatch.setattr(ksm, "SANDBOX_PROXY_HOST", "proxy.local")
 
@@ -886,7 +887,7 @@ def test_provision_conflicting_not_ready_pod_runs_startup_restore(
 ) -> None:
     import onyx.server.features.build.sandbox.kubernetes.kubernetes_sandbox_manager as ksm
 
-    monkeypatch.setattr(ksm, "SANDBOX_API_SERVER_URL", "http://api-server")
+    monkeypatch.setattr(ksm, "ONYX_SERVER_URL", "http://api-server")
     monkeypatch.setattr(ksm, "validate_sandbox_api_url", lambda *_: None)
     monkeypatch.setattr(ksm, "SANDBOX_PROXY_HOST", "proxy.local")
 
@@ -948,7 +949,7 @@ def test_provision_conflicting_not_ready_pod_restore_failure_does_not_cleanup(
 ) -> None:
     import onyx.server.features.build.sandbox.kubernetes.kubernetes_sandbox_manager as ksm
 
-    monkeypatch.setattr(ksm, "SANDBOX_API_SERVER_URL", "http://api-server")
+    monkeypatch.setattr(ksm, "ONYX_SERVER_URL", "http://api-server")
     monkeypatch.setattr(ksm, "validate_sandbox_api_url", lambda *_: None)
     monkeypatch.setattr(ksm, "SANDBOX_PROXY_HOST", "proxy.local")
 
diff --git a/backend/tests/unit/sandbox_proxy/test_onyx_pat_resolver.py b/backend/tests/unit/sandbox_proxy/test_onyx_pat_resolver.py
index 29271564b6..7dae26a034 100644
--- a/backend/tests/unit/sandbox_proxy/test_onyx_pat_resolver.py
+++ b/backend/tests/unit/sandbox_proxy/test_onyx_pat_resolver.py
@@ -1,6 +1,6 @@
 """Unit tests for `OnyxPatResolver`.
 
-Coverage: the host claim rule (incl. inert when `SANDBOX_API_SERVER_URL` is
+Coverage: the host claim rule (incl. inert when `ONYX_SERVER_URL` is
 unset), header rendering on both auth headers, and the fail-closed cases the
 dispatcher maps to a 403. The encrypt/store/read round-trip against a real DB
 is pinned in `tests/external_dependency_unit/sandbox_proxy/test_onyx_pat_resolver.py`.
@@ -70,7 +70,7 @@ def _ctx() -> InjectionContext:
 @pytest.fixture
 def resolver(monkeypatch: pytest.MonkeyPatch) -> OnyxPatResolver:
     # __init__ captures the API host, so the patch must precede construction.
-    monkeypatch.setattr(onyx_pat, "SANDBOX_API_SERVER_URL", _API_URL)
+    monkeypatch.setattr(onyx_pat, "ONYX_SERVER_URL", _API_URL)
     return OnyxPatResolver()
 
 
@@ -91,7 +91,7 @@ def test_claims_requires_matching_host_and_port(resolver: OnyxPatResolver) -> No
 
 
 def test_claims_matches_explicit_port(monkeypatch: pytest.MonkeyPatch) -> None:
-    monkeypatch.setattr(onyx_pat, "SANDBOX_API_SERVER_URL", "http://internal:8080")
+    monkeypatch.setattr(onyx_pat, "ONYX_SERVER_URL", "http://internal:8080")
     resolver = OnyxPatResolver()
     assert (
         resolver.claims(make_flow(host="internal", port=8080).request, _ctx()) is True
@@ -102,7 +102,7 @@ def test_claims_matches_explicit_port(monkeypatch: pytest.MonkeyPatch) -> None:
 
 
 def test_inert_when_api_url_unset(monkeypatch: pytest.MonkeyPatch) -> None:
-    monkeypatch.setattr(onyx_pat, "SANDBOX_API_SERVER_URL", "")
+    monkeypatch.setattr(onyx_pat, "ONYX_SERVER_URL", "")
     assert (
         OnyxPatResolver().claims(make_flow(host=_API_HOST, port=443).request, _ctx())
         is False
diff --git a/cli/README.md b/cli/README.md
index fcbc17b252..36539aa7e5 100644
--- a/cli/README.md
+++ b/cli/README.md
@@ -31,7 +31,8 @@ Environment variables override config file values:
 
 | Variable | Required | Description |
 |----------|----------|-------------|
-| `ONYX_SERVER_URL` | No | Server URL (default: `https://cloud.onyx.app`) |
+| `ONYX_SERVER_URL` | No | Server origin or already-prefixed API base (default: `https://cloud.onyx.app`) |
+| `ONYX_API_PREFIX` | No | API path prefix (default: `/api`); set to empty for direct backend access |
 | `ONYX_PAT` | No | Personal access token for authentication (required if no config file) |
 | `ONYX_PERSONA_ID` | No | Default agent/persona ID |
 | `ONYX_STREAM_MARKDOWN` | No | Enable/disable progressive markdown rendering (true/false) |
diff --git a/cli/internal/api/client.go b/cli/internal/api/client.go
index 0241cae1f9..26aa3a10f8 100644
--- a/cli/internal/api/client.go
+++ b/cli/internal/api/client.go
@@ -36,8 +36,8 @@ type Client struct {
 }
 
 // NewClient creates a new API client from config.
-// ServerURL is the server origin (e.g. "https://cloud.onyx.app").
-// APIURL appends the /api prefix to form the API base URL.
+// ServerURL may be a server origin or an API base that already includes the
+// configured API prefix.
 func NewClient(cfg config.OnyxCliConfig) *Client {
 	var transport *http.Transport
 	if t, ok := http.DefaultTransport.(*http.Transport); ok {
diff --git a/cli/internal/api/client_test.go b/cli/internal/api/client_test.go
index 5af9b9e514..56948f4146 100644
--- a/cli/internal/api/client_test.go
+++ b/cli/internal/api/client_test.go
@@ -29,7 +29,7 @@ func TestSearch_Success(t *testing.T) {
 		if r.Method != "POST" {
 			t.Errorf("method = %s, want POST", r.Method)
 		}
-		if !strings.HasSuffix(r.URL.Path, "/search") {
+		if r.URL.Path != "/api/search" {
 			t.Errorf("path = %s, want /api/search", r.URL.Path)
 		}
 		w.Header().Set("Content-Type", "application/json")
diff --git a/cli/internal/config/config.go b/cli/internal/config/config.go
index dff34ae25b..2e49956a2d 100644
--- a/cli/internal/config/config.go
+++ b/cli/internal/config/config.go
@@ -11,6 +11,7 @@ import (
 
 const (
 	EnvServerURL      = "ONYX_SERVER_URL"
+	EnvAPIPrefix      = "ONYX_API_PREFIX"
 	EnvAPIKey         = "ONYX_PAT"
 	EnvAgentID        = "ONYX_PERSONA_ID"
 	EnvSSHHostKey     = "ONYX_SSH_HOST_KEY"
@@ -56,18 +57,38 @@ func (c OnyxCliConfig) IsConfigured() bool {
 	return c.APIKey != ""
 }
 
-// APIURL appends the API prefix (default "/api") to the server origin.
-// Set ONYX_API_PREFIX="" for direct backend access without the proxy prefix.
-func APIURL(serverURL string) string {
+func apiPrefix() string {
 	prefix := "/api"
-	if v, ok := os.LookupEnv("ONYX_API_PREFIX"); ok {
-		prefix = v
+	if value, ok := os.LookupEnv(EnvAPIPrefix); ok {
+		prefix = value
 	}
-	u := strings.TrimRight(serverURL, "/")
+	return strings.Trim(prefix, "/")
+}
+
+// APIURL returns the API base for a server origin or an already-prefixed URL.
+// Set ONYX_API_PREFIX="" for direct backend access without a proxy path.
+func APIURL(serverURL string) string {
+	baseURL := strings.TrimRight(serverURL, "/")
+	prefix := apiPrefix()
 	if prefix == "" {
-		return u
+		return baseURL
 	}
-	return u + "/" + strings.Trim(prefix, "/")
+
+	suffix := "/" + prefix
+	if strings.HasSuffix(baseURL, suffix) {
+		return baseURL
+	}
+	return baseURL + suffix
+}
+
+// OnyxWebURL removes an API prefix when the configured URL already includes it.
+func OnyxWebURL(serverURL string) string {
+	baseURL := strings.TrimRight(serverURL, "/")
+	prefix := apiPrefix()
+	if prefix == "" {
+		return baseURL
+	}
+	return strings.TrimSuffix(baseURL, "/"+prefix)
 }
 
 // ConfigDir returns ~/.config/onyx-cli
diff --git a/cli/internal/config/config_test.go b/cli/internal/config/config_test.go
index 2bdbfb9def..3b41e1eef9 100644
--- a/cli/internal/config/config_test.go
+++ b/cli/internal/config/config_test.go
@@ -254,14 +254,16 @@ func TestSaveCreatesParentDirs(t *testing.T) {
 }
 
 func TestAPIURL(t *testing.T) {
+	t.Setenv(EnvAPIPrefix, "/api")
 	cases := []struct {
 		input string
 		want  string
 	}{
 		{"https://cloud.onyx.app", "https://cloud.onyx.app/api"},
 		{"https://cloud.onyx.app/", "https://cloud.onyx.app/api"},
+		{"https://cloud.onyx.app/api", "https://cloud.onyx.app/api"},
+		{"https://cloud.onyx.app/api/", "https://cloud.onyx.app/api"},
 		{"http://localhost:8080", "http://localhost:8080/api"},
-		{"http://localhost:3000", "http://localhost:3000/api"},
 	}
 	for _, tc := range cases {
 		got := APIURL(tc.input)
@@ -271,20 +273,42 @@ func TestAPIURL(t *testing.T) {
 	}
 }
 
+func TestAPIURLCustomPrefix(t *testing.T) {
+	t.Setenv(EnvAPIPrefix, "/onyx/api")
+	for _, input := range []string{
+		"https://onyx.example",
+		"https://onyx.example/onyx/api",
+	} {
+		got := APIURL(input)
+		if got != "https://onyx.example/onyx/api" {
+			t.Errorf("APIURL(%q) = %q", input, got)
+		}
+	}
+}
+
 func TestAPIURLEmptyPrefix(t *testing.T) {
-	t.Setenv("ONYX_API_PREFIX", "")
+	t.Setenv(EnvAPIPrefix, "")
+	if got := APIURL("http://localhost:8080/"); got != "http://localhost:8080" {
+		t.Errorf("APIURL() = %q", got)
+	}
+}
+
+func TestOnyxWebURL(t *testing.T) {
+	t.Setenv(EnvAPIPrefix, "/api")
 	cases := []struct {
 		input string
 		want  string
 	}{
-		{"http://localhost:8080", "http://localhost:8080"},
-		{"http://localhost:8080/", "http://localhost:8080"},
+		{"https://cloud.onyx.app/api", "https://cloud.onyx.app"},
+		{"https://cloud.onyx.app/api/", "https://cloud.onyx.app"},
+		{"https://onyx.example/base/api", "https://onyx.example/base"},
 		{"https://cloud.onyx.app", "https://cloud.onyx.app"},
+		{"http://localhost:8080", "http://localhost:8080"},
 	}
 	for _, tc := range cases {
-		got := APIURL(tc.input)
+		got := OnyxWebURL(tc.input)
 		if got != tc.want {
-			t.Errorf("APIURL(%q) = %q, want %q", tc.input, got, tc.want)
+			t.Errorf("OnyxWebURL(%q) = %q, want %q", tc.input, got, tc.want)
 		}
 	}
 }
diff --git a/cli/internal/embedded/SKILL.md b/cli/internal/embedded/SKILL.md
index 8066f700f3..1138bc7880 100644
--- a/cli/internal/embedded/SKILL.md
+++ b/cli/internal/embedded/SKILL.md
@@ -34,7 +34,8 @@ export ONYX_PAT="your-pat"
 
 | Variable          | Required | Description                                              |
 | ----------------- | -------- | -------------------------------------------------------- |
-| `ONYX_SERVER_URL` | No       | Onyx server URL (default: `https://cloud.onyx.app`) |
+| `ONYX_SERVER_URL` | No       | Server origin or already-prefixed API base (default: `https://cloud.onyx.app`) |
+| `ONYX_API_PREFIX` | No       | API path prefix (default: `/api`); empty for direct backend access |
 | `ONYX_PAT`    | Yes      | Personal access token for authentication (unless config file exists) |
 | `ONYX_PERSONA_ID` | No       | Default agent/persona ID                                 |
 | `ONYX_STREAM_MARKDOWN` | No | Enable/disable progressive markdown rendering (true/false) |
diff --git a/cli/internal/testutil/testutil.go b/cli/internal/testutil/testutil.go
index 16a2bc4a24..559b7e76cd 100644
--- a/cli/internal/testutil/testutil.go
+++ b/cli/internal/testutil/testutil.go
@@ -13,9 +13,11 @@ import (
 	"github.com/onyx-dot-app/onyx/cli/internal/iostreams"
 )
 
-// NewClient creates a test API client pointed at the given URL.
-func NewClient(url string) *api.Client {
-	return api.NewClient(config.OnyxCliConfig{ServerURL: url, APIKey: "test-key"})
+// NewClient creates a test API client pointed at the given server URL.
+func NewClient(serverURL string) *api.Client {
+	return api.NewClient(
+		config.OnyxCliConfig{ServerURL: serverURL, APIKey: "test-key"},
+	)
 }
 
 // StatusServer returns an httptest.Server that always responds with the given status code.
diff --git a/cli/internal/tui/commands.go b/cli/internal/tui/commands.go
index 3e5ffbcecd..60534dfa8a 100644
--- a/cli/internal/tui/commands.go
+++ b/cli/internal/tui/commands.go
@@ -49,7 +49,7 @@ func handleSlashCommand(m Model, text string) (Model, tea.Cmd) {
 		return cmdNew(m)
 
 	case "/connectors":
-		url := strings.TrimRight(m.config.ServerURL, "/") + "/admin/indexing/status"
+		url := config.OnyxWebURL(m.config.ServerURL) + "/admin/indexing/status"
 		if browser.OpenBrowser(url) {
 			m.viewport.addInfo("Opened " + url + " in browser")
 		} else {
@@ -58,7 +58,7 @@ func handleSlashCommand(m Model, text string) (Model, tea.Cmd) {
 		return m, nil
 
 	case "/settings":
-		url := strings.TrimRight(m.config.ServerURL, "/") + "/app/settings/general"
+		url := config.OnyxWebURL(m.config.ServerURL) + "/app/settings/general"
 		if browser.OpenBrowser(url) {
 			m.viewport.addInfo("Opened " + url + " in browser")
 		} else {
diff --git a/deployment/docker_compose/docker-compose.craft.yml b/deployment/docker_compose/docker-compose.craft.yml
index 836e203470..cc31bca154 100644
--- a/deployment/docker_compose/docker-compose.craft.yml
+++ b/deployment/docker_compose/docker-compose.craft.yml
@@ -8,9 +8,7 @@ services:
   api_server:
     environment:
       - SANDBOX_BACKEND=${SANDBOX_BACKEND:-docker}
-      # Public Onyx URL; Internal compose hostnames don't resolve from the
-      # sandbox bridge.
-      - SANDBOX_API_SERVER_URL=${SANDBOX_API_SERVER_URL:-}
+      - ONYX_SERVER_URL=${ONYX_SERVER_URL:-http://onyx-craft-api:8080}
       - SANDBOX_CONTAINER_IMAGE=${SANDBOX_CONTAINER_IMAGE:-onyxdotapp/sandbox:${IMAGE_TAG:-latest}}
       # Pinned: Must match the compose `networks:` block + install.sh literal.
       # An env_file leak would point Python at a non-existent network.
@@ -30,9 +28,10 @@ services:
     volumes:
       - ${SANDBOX_DOCKER_SOCKET:-/var/run/docker.sock}:/var/run/docker.sock
     networks:
-      # Bridge join lets api_server proxy the Next.js preview iframe.
-      - default
-      - onyx_craft_sandbox
+      default:
+      onyx_craft_sandbox:
+        aliases:
+          - onyx-craft-api
     # service_healthy, not service_started: The proxy binds its listener only
     # after initial sync, so service_started would race startup provisions.
     depends_on:
@@ -44,7 +43,7 @@ services:
       # Must match api_server so the idle-cleanup celery task uses the same
       # backend to snapshot + terminate sandboxes.
       - SANDBOX_BACKEND=${SANDBOX_BACKEND:-docker}
-      - SANDBOX_API_SERVER_URL=${SANDBOX_API_SERVER_URL:-}
+      - ONYX_SERVER_URL=${ONYX_SERVER_URL:-http://onyx-craft-api:8080}
       - SANDBOX_CONTAINER_IMAGE=${SANDBOX_CONTAINER_IMAGE:-onyxdotapp/sandbox:${IMAGE_TAG:-latest}}
       # See api_server above re: Pinned env_file-override vars.
       - SANDBOX_DOCKER_NETWORK=onyx_craft_sandbox
@@ -85,7 +84,7 @@ services:
       # OnyxPatResolver reads this at boot to know which host to claim for PAT
       # injection. Without it, /me requests pass through bare with the
       # placeholder bearer and api_server 403s.
-      - SANDBOX_API_SERVER_URL=${SANDBOX_API_SERVER_URL:-}
+      - ONYX_SERVER_URL=${ONYX_SERVER_URL:-http://onyx-craft-api:8080}
     volumes:
       - sandbox_proxy_ca:/var/lib/sandbox-proxy/ca
       # RO: the proxy only inspects (events watcher + initial sync).
diff --git a/deployment/docker_compose/env.template b/deployment/docker_compose/env.template
index b5647632bb..073faaa48a 100644
--- a/deployment/docker_compose/env.template
+++ b/deployment/docker_compose/env.template
@@ -21,15 +21,17 @@ IMAGE_TAG=latest
 ## kubernetes by image tag.
 # SANDBOX_BACKEND=docker
 #
-## SANDBOX_API_SERVER_URL must be a *public* HTTPS URL the sandbox can reach
-## the same way any other Onyx client does — internal compose hostnames like
-## "http://api_server:8080" do not resolve from inside the sandbox bridge.
-# SANDBOX_API_SERVER_URL=https://onyx.your-org.example
+## ONYX_SERVER_URL is the complete API base URL used by Onyx clients. The Craft
+## compose overlay defaults it to its private onyx-craft-api network alias,
+## which works on Docker Desktop and Linux without exposing another host port.
+## Override only when routing sandbox API traffic through a public reverse
+## proxy, including the /api path prefix served by that proxy.
+# ONYX_SERVER_URL=https://onyx.your-org.example/api
 #
 ## Sandbox bridge network. Created by install.sh (or manually:
 ##   docker network create onyx_craft_sandbox
-## Sandboxes join only this network — they cannot reach postgres, redis,
-## minio, or any other compose service by name.
+## Sandboxes join only this network. The firewall forces API and public egress
+## through sandbox-proxy; postgres, redis, and minio stay off the bridge.
 # SANDBOX_DOCKER_NETWORK=onyx_craft_sandbox
 #
 ## Per-sandbox container resource limits. Defaults match K8s pod *requests*
diff --git a/deployment/helm/charts/onyx/Chart.yaml b/deployment/helm/charts/onyx/Chart.yaml
index ce5a09249a..9ecd04da9c 100644
--- a/deployment/helm/charts/onyx/Chart.yaml
+++ b/deployment/helm/charts/onyx/Chart.yaml
@@ -5,7 +5,7 @@ home: https://www.onyx.app/
 sources:
   - "https://github.com/onyx-dot-app/onyx"
 type: application
-version: 0.7.2
+version: 0.7.3
 appVersion: latest
 annotations:
   category: Productivity
@@ -17,12 +17,9 @@ annotations:
       image: docker.io/onyxdotapp/onyx-backend:latest
   artifacthub.io/changes: |
     - kind: changed
-      description: The inference and indexing model servers now run on a distroless Docker
-        Hardened Image (no shell or package manager) as nonroot (the onyx user, UID 1001). Custom CA
-        certificates for the model servers are merged with certifi's public roots in Python
-        at startup instead of via update-ca-certificates. This chart version requires the
-        distroless model-server image — upgrade the chart and the model-server image
-        together (see values.yaml).
+      description: Replace configMap.SANDBOX_API_SERVER_URL with
+        configMap.ONYX_SERVER_URL for Craft sandbox API routing. Set it to the
+        exact API base, including /api when routing through the standard ingress.
 dependencies:
   # Helm uses the first condition path that exists: `postgresqlOperator.enabled`
   # is unset by default, so this falls through to `postgresql.enabled`. Set it
diff --git a/deployment/helm/charts/onyx/templates/craft-validation.yaml b/deployment/helm/charts/onyx/templates/craft-validation.yaml
index 75aba096bf..7b25967a95 100644
--- a/deployment/helm/charts/onyx/templates/craft-validation.yaml
+++ b/deployment/helm/charts/onyx/templates/craft-validation.yaml
@@ -5,8 +5,8 @@
 {{- if and $sandboxBackend (ne $sandboxBackend "kubernetes") }}
 {{- fail "configMap.SANDBOX_BACKEND must be \"kubernetes\" when configMap.ENABLE_CRAFT is enabled in the Helm chart" }}
 {{- end }}
-{{- if not (index .Values.configMap "SANDBOX_API_SERVER_URL") }}
-{{- fail "configMap.SANDBOX_API_SERVER_URL must be set when configMap.ENABLE_CRAFT is enabled" }}
+{{- if not (index .Values.configMap "ONYX_SERVER_URL") }}
+{{- fail "configMap.ONYX_SERVER_URL must be set when configMap.ENABLE_CRAFT is enabled" }}
 {{- end }}
 {{- $auth := .Values.auth | default dict }}
 {{- $sandboxPushSecret := (index $auth "sandboxPushSecret") | default dict }}
diff --git a/deployment/helm/charts/onyx/templates/sandbox-podtemplate.yaml b/deployment/helm/charts/onyx/templates/sandbox-podtemplate.yaml
index ba1a56fe95..0d4eb0ea22 100644
--- a/deployment/helm/charts/onyx/templates/sandbox-podtemplate.yaml
+++ b/deployment/helm/charts/onyx/templates/sandbox-podtemplate.yaml
@@ -25,7 +25,7 @@ kubelet evicts sandbox pods first under node disk pressure. */}}
 {{- $proxyPort := include "onyx.sandboxProxyPort" . }}
 {{- $proxyHost := include "onyx.sandboxProxyHost" . }}
 {{- $caConfigMap := (index $cm "SANDBOX_PROXY_CA_CONFIGMAP") | default "sandbox-proxy-ca-bundle" }}
-{{- $serverUrl := (index $cm "SANDBOX_API_SERVER_URL") }}
+{{- $serverUrl := (index $cm "ONYX_SERVER_URL") }}
 {{- $sandboxPod := .Values.sandboxPod | default dict }}
 {{- $caBundleFile := "/etc/ssl/sandbox/ca-bundle.crt" }}
 apiVersion: v1
@@ -140,6 +140,8 @@ template:
         env:
           - { name: ONYX_PAT, value: "replaced_by_egress_proxy" }
           - { name: ONYX_SERVER_URL, value: "{{ $serverUrl }}" }
+          {{/* The deployment value is the exact API base; do not append the CLI default. */}}
+          - { name: ONYX_API_PREFIX, value: "" }
           - { name: GH_TOKEN, value: "replaced_by_egress_proxy" }
           - { name: GH_NO_UPDATE_NOTIFIER, value: "1" }
           - { name: OPENCODE_DATA_HOME, value: "/workspace/opencode-data" }
diff --git a/deployment/helm/charts/onyx/values-ci.yaml b/deployment/helm/charts/onyx/values-ci.yaml
index c9ab0ccc37..4e7331460a 100644
--- a/deployment/helm/charts/onyx/values-ci.yaml
+++ b/deployment/helm/charts/onyx/values-ci.yaml
@@ -43,7 +43,7 @@ configMap:
   # No model server in this lane; skips the GPU-status probe that would hang API startup.
   DISABLE_MODEL_SERVER: "true"
   # Sandbox pods call the chart-managed API service, matching production.
-  SANDBOX_API_SERVER_URL: "http://onyx-api-service.onyx.svc.cluster.local:8080"
+  ONYX_SERVER_URL: "http://onyx-api-service.onyx.svc.cluster.local:8080"
   # Sandbox image the kind cluster pulls (built+pushed by the CI workflow).
   SANDBOX_CONTAINER_IMAGE: "localhost:5001/onyx-sandbox:ci"
   # Tiny requests so the sandbox pod schedules alongside the full Onyx stack on
diff --git a/deployment/helm/charts/onyx/values-localdev.yaml b/deployment/helm/charts/onyx/values-localdev.yaml
index b7e44bbaf3..797596c080 100644
--- a/deployment/helm/charts/onyx/values-localdev.yaml
+++ b/deployment/helm/charts/onyx/values-localdev.yaml
@@ -79,7 +79,8 @@ codeInterpreter:
 configMap:
   ENABLE_CRAFT: "true"
   # Host gateway (Docker Desktop), not internal cluster DNS; Linux-kind devs sub their own.
-  SANDBOX_API_SERVER_URL: "http://host.docker.internal:3000"
+  # Full base URL, path prefix included — the Next dev server proxies the API under /api.
+  ONYX_SERVER_URL: "http://host.docker.internal:3000/api"
   ENABLE_PAID_ENTERPRISE_EDITION_FEATURES: "true"
 
 sandboxProxy:
diff --git a/deployment/helm/charts/onyx/values.yaml b/deployment/helm/charts/onyx/values.yaml
index 6b4390364d..42a36287e2 100644
--- a/deployment/helm/charts/onyx/values.yaml
+++ b/deployment/helm/charts/onyx/values.yaml
@@ -1648,9 +1648,12 @@ configMap:
   SANDBOX_BACKEND: "kubernetes"
   SANDBOX_NAMESPACE: "onyx-sandboxes"
   SANDBOX_SERVICE_ACCOUNT_NAME: "sandbox"
+  # ONYX_SERVER_URL must be the full API base URL, path prefix included — e.g.
+  # "https://onyx.example/api" through the public proxy, or
+  # "http://<release>-api-service.<ns>.svc.cluster.local:8080" directly at the
+  # API service (no prefix). It is required when ENABLE_CRAFT=true.
   SANDBOX_PROXY_CA_SECRET: "sandbox-proxy-ca"
   SANDBOX_PROXY_CA_CONFIGMAP: "sandbox-proxy-ca-bundle"
-
 # -- Craft sandbox RBAC (rendered when configMap.ENABLE_CRAFT=true).
 craft:
   # Extra SAs (release ns) to also grant sandbox RBAC, e.g. a separate worker SA.
diff --git a/docs/craft/dev/local-kubernetes.md b/docs/craft/dev/local-kubernetes.md
index bff817ec95..a6d97d9ba9 100644
--- a/docs/craft/dev/local-kubernetes.md
+++ b/docs/craft/dev/local-kubernetes.md
@@ -371,7 +371,7 @@ For Craft development, the required vars (already in the template) are:
 ENABLE_CRAFT=true
 SANDBOX_BACKEND=kubernetes
 SANDBOX_CONTAINER_IMAGE=onyxdotapp/sandbox:dev
-SANDBOX_API_SERVER_URL=http://onyx-api-service.onyx.svc.cluster.local:8080
+ONYX_SERVER_URL=http://onyx-api-service.onyx.svc.cluster.local:8080
 ONYX_SANDBOX_PUSH_PRIVATE_KEY=AAAAAAAAAAAAAAAAAAAAAAAAAAAAAAAAAAAAAAAAAAA=
 ```
 
diff --git a/docs/craft/docker/docker-compose-overview.md b/docs/craft/docker/docker-compose-overview.md
index 7ec15b4828..11c077d95f 100644
--- a/docs/craft/docker/docker-compose-overview.md
+++ b/docs/craft/docker/docker-compose-overview.md
@@ -30,7 +30,6 @@ bash "$WT"/deployment/docker_compose/install.sh --local --include-craft
 cat >> ~/onyx_data/deployment/.env <<'ENV'
 ENABLE_CRAFT=true
 SANDBOX_BACKEND=docker
-SANDBOX_API_SERVER_URL=http://host.docker.internal:3001
 HOST_PORT=3001
 ENV
 
@@ -49,12 +48,8 @@ ENV
 
 ## Prerequisites
 
-- macOS with **Docker Desktop** (or OrbStack) — these provide `host.docker.internal`
-  resolution from inside the `onyx_craft_sandbox` bridge network, which the
-  sandbox container needs to reach api_server.
-- On Linux, replace `http://host.docker.internal:3001` with your machine's
-  reachable address (or use `--add-host` workarounds). Native Linux Docker
-  does *not* resolve `host.docker.internal` by default.
+- Docker Desktop, OrbStack, or Docker Engine on Linux. The Craft overlay uses
+  the private `onyx-craft-api` bridge alias on every platform.
 - ~80 GB free Docker disk. Onyx's full stack pulls ~30 GB; local image
   builds add another 10–15 GB; build cache balloons to 40+ GB if you let
   it. See [OpenSearch read-only block](#opensearch-flipped-into-read-only-mode-disk-full) below.
@@ -70,7 +65,7 @@ These must end up in `~/onyx_data/deployment/.env` after install:
 |---|---|---|
 | `ENABLE_CRAFT=true` | yes | `--include-craft` sets this (fresh installs and existing `.env`). |
 | `SANDBOX_BACKEND=docker` | yes | `--include-craft` sets this alongside `ENABLE_CRAFT`. |
-| `SANDBOX_API_SERVER_URL=http://host.docker.internal:3001` | yes | Provision raises `ValueError("SANDBOX_API_SERVER_URL must be set")` without it. Must be a URL the sandbox container can reach **from the `onyx_craft_sandbox` bridge** — compose-internal hostnames (`api_server`, `nginx`) won't resolve there. Match the port to `HOST_PORT`. |
+| `ONYX_SERVER_URL` | optional | Complete API base URL. The Craft overlay defaults to `http://onyx-craft-api:8080` on the private sandbox bridge. Override with a public URL only when desired, including its `/api` path prefix. |
 | `HOST_PORT=3001` | only if 3000 conflicts | Default is 3000; nginx binds this on the host. Free up 3000 or change here. |
 | `IMAGE_TAG` | optional | Uses the normal compose default (`latest`) unless set. Craft uses this same tag for the sandbox image, so do not set a separate sandbox image for normal deployments. There are **no** Craft-specific app/backend images — Craft is enabled at runtime via `ENABLE_CRAFT=true` (above). See [image architecture](../infra/image-architecture.md). |
 | `ONYX_BACKEND_IMAGE` | only when running unreleased PRs | Lets you override just the backend image without forcing model-server / web-server to the same tag. |
@@ -122,12 +117,11 @@ adapt the prompts (Standard mode = `2`, keep existing env = blank).
 ### 3. Fix the .env
 
 On an existing `.env`, `--include-craft` writes `ENABLE_CRAFT=true` and
-`SANDBOX_BACKEND=docker` for you (on both the update and restart paths). It
-does **not** set the host-specific values, so append those yourself:
+`SANDBOX_BACKEND=docker` for you (on both the update and restart paths).
+Set `HOST_PORT` only when the default port is unavailable:
 
 ```bash
 cat >> ~/onyx_data/deployment/.env <<'ENV'
-SANDBOX_API_SERVER_URL=http://host.docker.internal:3001
 HOST_PORT=3001
 ENV
 ```
diff --git a/docs/craft/features/egress-proxy-and-approvals/README.md b/docs/craft/features/egress-proxy-and-approvals/README.md
index c6859e2876..a0d2c4ae59 100644
--- a/docs/craft/features/egress-proxy-and-approvals/README.md
+++ b/docs/craft/features/egress-proxy-and-approvals/README.md
@@ -491,7 +491,7 @@ The proxy uses first-claim-wins credential dispatch. Resolvers must keep
 ### Onyx PAT Resolver
 
 `OnyxPatResolver` claims requests whose host and port match
-`SANDBOX_API_SERVER_URL`.
+`ONYX_SERVER_URL`.
 
 It loads the sandbox row and decrypts `Sandbox.encrypted_pat`, then injects both
 Onyx API key header names as bearer tokens. The tenant is embedded in the PAT,
@@ -747,7 +747,8 @@ Relevant config:
 
 - `ENABLE_CRAFT=true` enables Craft chart resources.
 - `SANDBOX_BACKEND` is `kubernetes` or `docker`.
-- `SANDBOX_API_SERVER_URL` must be set for sandbox API calls and PAT injection.
+- `ONYX_SERVER_URL` must be the complete API base for sandbox API calls and PAT
+  injection.
 - `SANDBOX_PROXY_HOST` and `SANDBOX_PROXY_PORT` tell sandboxes where to proxy.
 - `SANDBOX_PROXY_LISTEN_PORT` and `SANDBOX_PROXY_HEALTHZ_PORT` configure the
   proxy process.
diff --git a/docs/craft/kubernetes/craft-eks-runbook.md b/docs/craft/kubernetes/craft-eks-runbook.md
index 3e54a20f37..430bf8d965 100644
--- a/docs/craft/kubernetes/craft-eks-runbook.md
+++ b/docs/craft/kubernetes/craft-eks-runbook.md
@@ -210,7 +210,7 @@ sandboxProxy:
 - ElastiCache: `REDIS_HOST`, `REDIS_SSL=true`, `REDIS_SSL_CERT_REQS=none`, `auth.redis.enabled=false` (no auth token).
 - OpenSearch (v4.0 search backend): `ONYX_DISABLE_VESPA=true`, `ENABLE_OPENSEARCH_INDEXING/RETRIEVAL_FOR_ONYX=true`, `USING_AWS_MANAGED_OPENSEARCH=true`, `OPENSEARCH_REST_API_PORT=443`, `OPENSEARCH_USE_SSL=true`, `OPENSEARCH_ADMIN_USERNAME=admin`.
 - S3: `S3_FILE_STORE_BUCKET_NAME`, `S3_ENDPOINT_URL=""`, `AWS_REGION_NAME`.
-- Craft: `ENABLE_CRAFT=true`, `SANDBOX_API_SERVER_URL=http://onyx-api-service.onyx.svc.cluster.local:8080`, `auth.sandboxPushSecret.enabled=true`. (`SANDBOX_SERVICE_ACCOUNT_NAME`/`SANDBOX_CONTAINER_IMAGE` default correctly.)
+- Craft: `ENABLE_CRAFT=true`, `ONYX_SERVER_URL=http://onyx-api-service.onyx.svc.cluster.local:8080`, `auth.sandboxPushSecret.enabled=true`. (`SANDBOX_SERVICE_ACCOUNT_NAME`/`SANDBOX_CONTAINER_IMAGE` default correctly.)
 
 ### Images
 Use an immutable release tag for Kubernetes customer Craft deployments, e.g.