diff --git a/litellm/proxy/proxy_server.py b/litellm/proxy/proxy_server.py
index 698c1e6e752..050b0a7e60c 100644
--- a/litellm/proxy/proxy_server.py
+++ b/litellm/proxy/proxy_server.py
@@ -2729,6 +2729,58 @@ try:
         except (PermissionError, OSError) as e:
             return False, str(e)
 
+    def _rewrite_ui_config_path(content: str, server_root_path: str) -> str:
+        """
+        Point the UI's config request at server_root_path, keeping already-rewritten paths.
+
+        The UI files are rewritten in place on every startup, and when server_root_path ends
+        in /litellm the rewritten path still contains the original one, so a plain replace
+        would prepend the root path again on each restart.
+        """
+        ui_config_path: Final = f"{server_root_path}/.well-known/litellm-ui-config"
+        return ui_config_path.join(
+            part.replace("/litellm/.well-known/litellm-ui-config", ui_config_path)
+            for part in content.split(ui_config_path)
+        )
+
+    def _apply_server_root_path_to_ui(ui_dir: str, server_root_path: str) -> None:
+        for root, _dirs, files in os.walk(ui_dir):
+            for filename in files:
+                file_path = os.path.join(root, filename)
+                # Skip binary files and files that don't need path replacement
+                if filename.endswith(
+                    (
+                        ".png",
+                        ".jpg",
+                        ".jpeg",
+                        ".gif",
+                        ".ico",
+                        ".woff",
+                        ".woff2",
+                        ".ttf",
+                        ".eot",
+                    )
+                ):
+                    continue
+                try:
+                    with open(file_path, "r", encoding="utf-8") as f:
+                        content = f.read()
+
+                    # Replace the asset prefix with the server root path
+                    modified_content = content.replace(
+                        f"{litellm_asset_prefix}",
+                        f"{server_root_path}",
+                    )
+
+                    # Replace the /.well-known/litellm-ui-config with the server root path
+                    modified_content = _rewrite_ui_config_path(modified_content, server_root_path)
+
+                    with open(file_path, "w", encoding="utf-8") as f:
+                        f.write(modified_content)
+                except (UnicodeDecodeError, PermissionError, OSError):
+                    # Skip binary files or files we can't write to
+                    continue
+
     # Use a writable runtime UI directory whenever possible.
     # This prevents mutating the packaged UI directory (e.g. site-packages or the repo checkout)
     # and ensures extensionless routes like /ui/login work via <route>/index.html.
@@ -2814,46 +2866,7 @@ try:
                 ui_path,
             )
         else:
-            # Iterate through files in the UI directory
-            for root, dirs, files in os.walk(ui_path):
-                for filename in files:
-                    file_path = os.path.join(root, filename)
-                    # Skip binary files and files that don't need path replacement
-                    if filename.endswith(
-                        (
-                            ".png",
-                            ".jpg",
-                            ".jpeg",
-                            ".gif",
-                            ".ico",
-                            ".woff",
-                            ".woff2",
-                            ".ttf",
-                            ".eot",
-                        )
-                    ):
-                        continue
-                    try:
-                        with open(file_path, "r", encoding="utf-8") as f:
-                            content = f.read()
-
-                        # Replace the asset prefix with the server root path
-                        modified_content = content.replace(
-                            f"{litellm_asset_prefix}",
-                            f"{server_root_path}",
-                        )
-
-                        # Replace the /.well-known/litellm-ui-config with the server root path
-                        modified_content = modified_content.replace(
-                            "/litellm/.well-known/litellm-ui-config",
-                            f"{server_root_path}/.well-known/litellm-ui-config",
-                        )
-
-                        with open(file_path, "w", encoding="utf-8") as f:
-                            f.write(modified_content)
-                    except (UnicodeDecodeError, PermissionError, OSError):
-                        # Skip binary files or files we can't write to
-                        continue
+            _apply_server_root_path_to_ui(ui_path, server_root_path)
 
     # # Mount the _next directory at the root level
     app.mount(
diff --git a/tests/unit/proxy/test_proxy_server.py b/tests/unit/proxy/test_proxy_server.py
index a50db09128f..dd638618ddf 100644
--- a/tests/unit/proxy/test_proxy_server.py
+++ b/tests/unit/proxy/test_proxy_server.py
@@ -3246,6 +3246,26 @@ def test_non_root_ui_path_logic(monkeypatch, tmp_path, ui_exists, ui_has_content
         assert mock_logger.info.call_count == 0
 
 
+@pytest.mark.parametrize("server_root_path", ["/foo", "/litellm", "/foo/litellm"])
+def test_server_root_path_ui_rewrite_is_stable_across_restarts(tmp_path, server_root_path):
+    from litellm.proxy.proxy_server import _apply_server_root_path_to_ui
+
+    chunk = tmp_path / "_next" / "static" / "chunks" / "app.js"
+    chunk.parent.mkdir(parents=True)
+    chunk.write_text(
+        'fetch(`${g}/litellm/.well-known/litellm-ui-config`);const u={url:"/litellm/.well-known/litellm-ui-config"}',
+        encoding="utf-8",
+    )
+
+    for _ in range(3):
+        _apply_server_root_path_to_ui(str(tmp_path), server_root_path)
+
+    assert chunk.read_text(encoding="utf-8") == (
+        f"fetch(`${{g}}{server_root_path}/.well-known/litellm-ui-config`);"
+        f'const u={{url:"{server_root_path}/.well-known/litellm-ui-config"}}'
+    )
+
+
 @pytest.mark.asyncio
 async def test_get_config_callbacks_with_all_types(client_no_auth):
     """