diff --git a/fixtures/apidocs_test_case.py b/fixtures/apidocs_test_case.py
index a8b78947d371..e7fab77e297a 100644
--- a/fixtures/apidocs_test_case.py
+++ b/fixtures/apidocs_test_case.py
@@ -1,5 +1,6 @@
 import functools
 import os
+from urllib.parse import urlsplit
 
 import orjson
 from django.conf import settings
@@ -22,7 +23,9 @@ def _load_schema() -> Spec:
     path = os.path.join(os.path.dirname(__file__), "../tests/apidocs/openapi-derefed.json")
     with open(path, "rb") as json_file:
         data = orjson.loads(json_file.read())
-    data["servers"][0]["url"] = settings.SENTRY_OPTIONS["system.url-prefix"]
+    server = data["servers"][0]
+    # Paths are relative to the server URL's path, so keep it.
+    server["url"] = settings.SENTRY_OPTIONS["system.url-prefix"] + urlsplit(server["url"]).path
     del data["components"]
     return Spec.from_dict(data)
 
diff --git a/src/sentry/api/base.py b/src/sentry/api/base.py
index 36e421d99ed2..246e3d5d05f6 100644
--- a/src/sentry/api/base.py
+++ b/src/sentry/api/base.py
@@ -305,6 +305,7 @@ class Endpoint(APIView):
     idempotent_methods: frozenset[HTTP_METHOD_NAME] | None = None
     rate_limits: RateLimitConfig | Callable[..., RateLimitConfig] = DEFAULT_RATE_LIMIT_CONFIG
     enforce_rate_limit: bool = settings.SENTRY_RATELIMITER_ENABLED
+    # Origins that serve this endpoint, for the API docs; the schema build adds the base path.
     servers: list[dict[str, Any]] | None = None
     # For endpoints people may call with any credential, API tokens included, but a caller
     # with no user (e.g. a service account) may not: it gets a 403 user-required, counted
diff --git a/src/sentry/apidocs/hooks.py b/src/sentry/apidocs/hooks.py
index 474fbd4d1847..001e2d539373 100644
--- a/src/sentry/apidocs/hooks.py
+++ b/src/sentry/apidocs/hooks.py
@@ -4,6 +4,7 @@
 from collections import OrderedDict
 from collections.abc import Callable, Mapping
 from typing import Any, Literal, NotRequired, TypedDict, cast
+from urllib.parse import urlsplit
 
 from django.http import HttpResponseBase
 from drf_spectacular.generators import EndpointEnumerator, SchemaGenerator
@@ -434,6 +435,28 @@ def custom_postprocessing_hook(
     return result
 
 
+def relative_paths_hook(result: dict[str, Any], generator: Any, **kwargs: Any) -> dict[str, Any]:
+    """Make every path relative to the path of the first server URL, the API base path.
+
+    Clients then read the base path, and the API version in it, from `servers` instead of
+    from each path. An endpoint's `servers` name origins, so they get the base path too.
+    """
+    base_path = urlsplit(result["servers"][0]["url"]).path.rstrip("/")
+    paths = {}
+    for path, path_item in result["paths"].items():
+        if not path.startswith(f"{base_path}/"):
+            raise SentryApiBuildError(f"{path} is not under the API base path {base_path}.")
+        for operation in path_item.values():
+            if isinstance(operation, dict) and "servers" in operation:
+                # New dicts: the originals are the endpoint class's own `servers`.
+                operation["servers"] = [
+                    {**server, "url": server["url"] + base_path} for server in operation["servers"]
+                ]
+        paths[path.removeprefix(base_path)] = path_item
+    result["paths"] = paths
+    return result
+
+
 def _check_tag(method_info: Mapping[str, Any], endpoint_name: str) -> None:
     if method_info.get("tags") is None:
         raise SentryApiBuildError(
diff --git a/src/sentry/conf/api_base_path.py b/src/sentry/conf/api_base_path.py
new file mode 100644
index 000000000000..a3826c99b8b1
--- /dev/null
+++ b/src/sentry/conf/api_base_path.py
@@ -0,0 +1,4 @@
+# The versioned API's mount point. The URL conf mounts sentry.api.urls here, and the
+# API docs put it in the spec's server URL, so clients read it, and the version in it,
+# from the spec instead of hard-coding it.
+API_BASE_PATH = "/api/0"
diff --git a/src/sentry/conf/server.py b/src/sentry/conf/server.py
index f8a01f3a362b..8806ab764ff8 100644
--- a/src/sentry/conf/server.py
+++ b/src/sentry/conf/server.py
@@ -19,6 +19,7 @@
 
 import sentry
 import sentry.utils.types as env_types
+from sentry.conf import api_base_path
 from sentry.conf.api_pagination_allowlist_do_not_modify import (
     SENTRY_API_PAGINATION_ALLOWLIST_DO_NOT_MODIFY,
 )
@@ -1510,11 +1511,14 @@ def custom_parameter_sort(parameter: _OperationParameter) -> tuple[str, int]:
         "POSTPROCESSING_HOOKS": [
             "sentry.apidocs.hooks.custom_postprocessing_hook",
             "drf_spectacular.hooks.postprocess_schema_enum_id_removal",
+            # Last, so the hooks above see full paths.
+            "sentry.apidocs.hooks.relative_paths_hook",
         ],
         "PREPROCESSING_HOOKS": ["sentry.apidocs.hooks.custom_preprocessing_hook"],
         "SERVERS": [
             {
-                "url": "https://{region}.sentry.io",
+                # The path is the API base path; operation paths are relative to it.
+                "url": f"https://{{region}}.sentry.io{api_base_path.API_BASE_PATH}",
                 "variables": {
                     "region": {
                         "default": "us",
diff --git a/src/sentry/web/urls.py b/src/sentry/web/urls.py
index da825a0828a1..876c13b34c56 100644
--- a/src/sentry/web/urls.py
+++ b/src/sentry/web/urls.py
@@ -14,6 +14,7 @@
 from sentry.api.endpoints.warmup import WarmupEndpoint
 from sentry.auth.providers.saml2.provider import SAML2AcceptACSView, SAML2MetadataView, SAML2SLSView
 from sentry.charts.endpoints import serve_chartcuterie_config
+from sentry.conf.api_base_path import API_BASE_PATH
 from sentry.conf.types.sentry_config import SentryMode
 from sentry.feedback.endpoints.error_page_embed import ErrorPageEmbedView
 from sentry.integrations.web.doc_integration_avatar import DocIntegrationAvatarPhotoView
@@ -181,8 +182,10 @@
         name="get_cli_download_url",
     ),
     # Versioned API
+    # A regex route, not path(): route strings such as "^api/0/users/$" feed analytics and
+    # generated silo URL lists.
     re_path(
-        r"^api/0/",
+        rf"^{re.escape(API_BASE_PATH.removeprefix('/'))}/",
         include("sentry.api.urls"),
     ),
     # Legacy unversioned endpoints
diff --git a/tests/apidocs/endpoints/integration_platform/test_group_integration_details.py b/tests/apidocs/endpoints/integration_platform/test_group_integration_details.py
index 60b443f8a519..deeddba0d037 100644
--- a/tests/apidocs/endpoints/integration_platform/test_group_integration_details.py
+++ b/tests/apidocs/endpoints/integration_platform/test_group_integration_details.py
@@ -66,7 +66,7 @@ def test_put(self) -> None:
 
         self.validate_schema(request, response)
         schema = self.cached_schema.content()["paths"][
-            "/api/0/organizations/{organization_id_or_slug}/issues/{issue_id}/integrations/{integration_id}/"
+            "/organizations/{organization_id_or_slug}/issues/{issue_id}/integrations/{integration_id}/"
         ]["put"]["requestBody"]["content"]["application/json"]["schema"]
         assert {"externalIssue", "repo", "comment"} <= schema["properties"].keys()
         assert schema["required"] == ["externalIssue"]
diff --git a/tests/apidocs/endpoints/integration_platform/test_sentry_app_external_issues.py b/tests/apidocs/endpoints/integration_platform/test_sentry_app_external_issues.py
index a513efcf2247..acb49213b7f1 100644
--- a/tests/apidocs/endpoints/integration_platform/test_sentry_app_external_issues.py
+++ b/tests/apidocs/endpoints/integration_platform/test_sentry_app_external_issues.py
@@ -73,7 +73,7 @@ def test_issue_link_action(self) -> None:
         self.validate_schema(RequestFactory().post(url, data), response)
 
         request_body = self.cached_schema.content()["paths"][
-            "/api/0/sentry-app-installations/{uuid}/external-issue-actions/"
+            "/sentry-app-installations/{uuid}/external-issue-actions/"
         ]["post"]["requestBody"]
         assert request_body["required"] is True
         schema = request_body["content"]["application/json"]["schema"]
diff --git a/tests/apidocs/test_hooks.py b/tests/apidocs/test_hooks.py
index e7e9de30d17a..e7dc7e8c4adc 100644
--- a/tests/apidocs/test_hooks.py
+++ b/tests/apidocs/test_hooks.py
@@ -20,6 +20,7 @@
     _fix_nullable_enums,
     custom_postprocessing_hook,
     custom_preprocessing_hook,
+    relative_paths_hook,
 )
 from sentry.apidocs.utils import SentryApiBuildError
 from sentry.core.endpoints.organization_index import OrganizationIndexEndpoint
@@ -96,6 +97,35 @@ def test_servers_applied_to_endpoint(self) -> None:
         assert "servers" not in processed["paths"]["/api/0/other/endpoint/"]["get"]
 
 
+class RelativePathsHookTest(TestCase):
+    def test_paths_are_relative_to_the_server_path(self) -> None:
+        endpoint_servers = [{"url": "https://{region}.sentry.io"}]
+        result = {
+            "servers": [{"url": "https://{region}.sentry.io/api/0"}],
+            "paths": {
+                "/api/0/seer/models/": {"get": {"servers": endpoint_servers}},
+                "/api/0/organizations/": {"get": {}},
+            },
+        }
+
+        processed = relative_paths_hook(result, None)
+
+        assert processed["paths"] == {
+            "/seer/models/": {"get": {"servers": [{"url": "https://{region}.sentry.io/api/0"}]}},
+            "/organizations/": {"get": {}},
+        }
+        assert endpoint_servers == [{"url": "https://{region}.sentry.io"}]
+
+    def test_rejects_a_path_outside_the_base_path(self) -> None:
+        result = {
+            "servers": [{"url": "https://{region}.sentry.io/api/0"}],
+            "paths": {"/oauth/token/": {}},
+        }
+
+        with pytest.raises(SentryApiBuildError, match="not under the API base path /api/0"):
+            relative_paths_hook(result, None)
+
+
 class PublishStatusFilterTest(TestCase):
     """Only published statuses reach the OpenAPI pipeline, and PUBLIC_EXPERIMENTAL is marked."""