diff --git a/litellm/proxy/_experimental/mcp_server/oauth_utils.py b/litellm/proxy/_experimental/mcp_server/oauth_utils.py
index 6cea56dd5d3..dd2be348b76 100644
--- a/litellm/proxy/_experimental/mcp_server/oauth_utils.py
+++ b/litellm/proxy/_experimental/mcp_server/oauth_utils.py
@@ -180,6 +180,22 @@ def well_known_root_suffix() -> str:
     return "" if root == "/" else root
 
 
+def get_route_relative_request_path(scope: Scope) -> str:
+    """The request path the MCP route shapes are written against: the raw ASGI path with the
+    deployment's ``root_path`` removed.
+
+    ``scope["path"]`` and ``_original_path`` are both raw request-line paths, so on a sub-path
+    deployment they still carry the ``SERVER_ROOT_PATH`` prefix (``/litellm/{server}/mcp``) while
+    every route shape compared against them is root-relative. Mirrors the segment-boundary strip in
+    :func:`litellm.proxy.auth.auth_utils.get_request_route`, which the rest of the MCP auth path
+    already routes through, so ``/litellmfoo`` is not truncated under ``root_path=/litellm``."""
+    raw_path = str(scope.get("_original_path") or scope.get("path", "") or "")
+    root_path = str(scope.get("app_root_path") or scope.get("root_path") or "").rstrip("/")
+    if root_path and (raw_path == root_path or raw_path.startswith(f"{root_path}/")):
+        return raw_path[len(root_path) :]
+    return raw_path
+
+
 def get_passthrough_resource_metadata_url(scope: Scope, server_name: str) -> str:
     """The per-server protected-resource metadata URL matching the spelling the request
     arrived on, so a strict RFC 9728 client resolves the same route the proxy registered.
@@ -188,7 +204,7 @@ def get_passthrough_resource_metadata_url(scope: Scope, server_name: str) -> str
     the route decorators insert it (see :func:`well_known_root_suffix`)."""
     request = Request(scope)
     base_url = get_request_base_url(request)
-    _path = scope.get("_original_path") or scope.get("path", "") or ""
+    _path = get_route_relative_request_path(scope)
 
     if _path.startswith(f"/{server_name}/mcp"):
         return f"{base_url}/.well-known/oauth-protected-resource{well_known_root_suffix()}/{server_name}/mcp"
diff --git a/tests/test_litellm/proxy/_experimental/mcp_server/auth/test_user_api_key_auth_mcp.py b/tests/test_litellm/proxy/_experimental/mcp_server/auth/test_user_api_key_auth_mcp.py
index 0b95a497882..06e8ff8e71d 100644
--- a/tests/test_litellm/proxy/_experimental/mcp_server/auth/test_user_api_key_auth_mcp.py
+++ b/tests/test_litellm/proxy/_experimental/mcp_server/auth/test_user_api_key_auth_mcp.py
@@ -6314,6 +6314,49 @@ async def test_per_server_challenge_for_gateway_managed_oauth2(self):
             www_authenticate = (exc_info.value.headers or {})["WWW-Authenticate"]
             assert www_authenticate == f'Bearer resource_metadata="http://testserver{expected_metadata_path}"'
 
+    async def test_per_server_challenge_keeps_spelling_under_server_root_path(self):
+        """On a sub-path deployment the challenge must still advertise the spelling the client
+        used. ``_original_path`` is a raw request-line path, so under SERVER_ROOT_PATH it reads
+        ``/litellm/{server}/mcp``; matching that against the root-relative ``/{server}/mcp`` shape
+        used to fail, silently pointing a legacy-spelling client at the standard-pattern document
+        whose ``resource`` is ``{base}/mcp/{server}`` rather than the ``{base}/{server}/mcp`` URL it
+        called, which a strict RFC 9728 section 3 client rejects."""
+        import os
+
+        from litellm.types.mcp import MCPAuth
+        from litellm.types.mcp_server.mcp_server_manager import MCPServer
+
+        server = MCPServer(
+            server_id="gh-id",
+            name="github",
+            server_name="github",
+            url="https://upstream.example/mcp",
+            transport="http",
+            auth_type=MCPAuth.oauth2,
+        )
+        for original_path, expected_metadata_path in (
+            ("/litellm/mcp/github", "/litellm/.well-known/oauth-protected-resource/litellm/mcp/github"),
+            ("/litellm/github/mcp", "/litellm/.well-known/oauth-protected-resource/litellm/github/mcp"),
+        ):
+            scope = {
+                **self._scope(path="/mcp/github"),
+                "root_path": "/litellm",
+                "_original_path": original_path,
+            }
+            with (
+                patch.dict(os.environ, {"SERVER_ROOT_PATH": "/litellm"}),
+                patch(self._AUTH_PATCH_TARGET, side_effect=self._auth_401()),
+                patch(
+                    "litellm.proxy._experimental.mcp_server.mcp_server_manager.global_mcp_server_manager"
+                ) as mock_mgr,
+            ):
+                mock_mgr.get_mcp_server_by_name.return_value = server
+                with pytest.raises(HTTPException) as exc_info:
+                    await MCPRequestHandler.process_mcp_request(scope)
+            assert exc_info.value.status_code == 401
+            www_authenticate = (exc_info.value.headers or {})["WWW-Authenticate"]
+            assert www_authenticate == f'Bearer resource_metadata="http://testserver{expected_metadata_path}"'
+
     async def test_no_per_server_challenge_for_non_gateway_managed_targets(self):
         """The per-server challenge fires only for the server set the gateway's keyless flow
         serves: an OBO server and a multi-server CSV path keep the original admission error