diff --git a/litellm/llms/github_copilot/authenticator.py b/litellm/llms/github_copilot/authenticator.py
index 27a4651f154..2b96ee6d79a 100644
--- a/litellm/llms/github_copilot/authenticator.py
+++ b/litellm/llms/github_copilot/authenticator.py
@@ -4,6 +4,8 @@ import time
 from typing import Final
 
 import httpx
+from pydantic import TypeAdapter, ValidationError
+from typing_extensions import TypedDict
 
 from litellm._logging import verbose_logger
 from litellm.llms.custom_httpx.http_handler import _get_httpx_client
@@ -15,6 +17,17 @@ from .common_utils import (
     get_copilot_auth_headers,
 )
 
+
+class _LegacyCopilotEndpoints(TypedDict, total=False):
+    api: str
+
+
+class _LegacyCopilotTokenCache(TypedDict, total=False):
+    endpoints: _LegacyCopilotEndpoints
+
+
+_LEGACY_COPILOT_TOKEN_CACHE_ADAPTER = TypeAdapter(_LegacyCopilotTokenCache)
+
 # Constants (default values — overridable via environment variables at call time)
 DEFAULT_GITHUB_CLIENT_ID: Final = "Iv1.b507a08c87ecfe98"
 DEFAULT_GITHUB_DEVICE_CODE_URL: Final = "https://github.com/login/device/code"
@@ -33,6 +46,14 @@ class Authenticator:
             self.token_dir,
             os.getenv("GITHUB_COPILOT_ACCESS_TOKEN_FILE", "access-token"),
         )
+        self.legacy_api_key_file = os.path.join(
+            self.token_dir,
+            os.getenv("GITHUB_COPILOT_API_KEY_FILE", "api-key.json"),
+        )
+        if os.getenv("GITHUB_COPILOT_API_KEY_URL"):
+            verbose_logger.warning(
+                "GITHUB_COPILOT_API_KEY_URL is no longer used; LiteLLM sends the OAuth access token directly"
+            )
         self._ensure_token_dir()
 
     def get_access_token(self) -> str:
@@ -82,7 +103,18 @@ class Authenticator:
             )
 
     def get_api_base(self) -> str | None:
-        return os.getenv("GITHUB_COPILOT_API_BASE")
+        configured_api_base = os.getenv("GITHUB_COPILOT_API_BASE")
+        if configured_api_base:
+            return configured_api_base
+        try:
+            with open(self.legacy_api_key_file, "r") as legacy_api_key_file:
+                legacy_cache = _LEGACY_COPILOT_TOKEN_CACHE_ADAPTER.validate_json(legacy_api_key_file.read())
+        except IOError:
+            return None
+        except ValidationError as e:
+            verbose_logger.warning(f"Error reading legacy GitHub Copilot API endpoint: {str(e)}")
+            return None
+        return legacy_cache.get("endpoints", {}).get("api")
 
     def _ensure_token_dir(self) -> None:
         """Ensure the token directory exists."""
diff --git a/tests/test_litellm/llms/github_copilot/test_github_copilot_authenticator.py b/tests/test_litellm/llms/github_copilot/test_github_copilot_authenticator.py
index 7b42a774b43..422b5e7dfbe 100644
--- a/tests/test_litellm/llms/github_copilot/test_github_copilot_authenticator.py
+++ b/tests/test_litellm/llms/github_copilot/test_github_copilot_authenticator.py
@@ -41,6 +41,7 @@ class TestGitHubCopilotAuthenticator:
             auth = Authenticator()
             assert auth.token_dir.endswith("/github_copilot")
             assert auth.access_token_file.endswith("/access-token")
+            assert auth.legacy_api_key_file.endswith("/api-key.json")
             mock_makedirs.assert_called_once()
 
     def test_ensure_token_dir(self):
@@ -52,6 +53,42 @@ class TestGitHubCopilotAuthenticator:
             auth = Authenticator()
             mock_makedirs.assert_called_once_with(auth.token_dir, exist_ok=True)
 
+    def test_get_api_base_prefers_environment(self, authenticator):
+        with (
+            patch.dict(
+                os.environ,
+                {"GITHUB_COPILOT_API_BASE": "https://configured.githubcopilot.example"},
+                clear=True,
+            ),
+            patch("builtins.open", mock_open()) as mock_file,
+        ):
+            assert authenticator.get_api_base() == "https://configured.githubcopilot.example"
+            mock_file.assert_not_called()
+
+    def test_get_api_base_uses_legacy_endpoint(self, authenticator):
+        legacy_cache = '{"token":"ignored","endpoints":{"api":"https://api.enterprise.githubcopilot.com"}}'
+        with (
+            patch.dict(os.environ, {}, clear=True),
+            patch("builtins.open", mock_open(read_data=legacy_cache)),
+        ):
+            assert authenticator.get_api_base() == "https://api.enterprise.githubcopilot.com"
+
+    def test_deprecated_api_key_url_warns(self):
+        with (
+            patch.dict(
+                os.environ,
+                {"GITHUB_COPILOT_API_KEY_URL": "https://deprecated.example.com/token"},
+                clear=True,
+            ),
+            patch("os.path.exists", return_value=True),
+            patch("litellm.llms.github_copilot.authenticator.verbose_logger.warning") as mock_warning,
+        ):
+            Authenticator()
+
+        mock_warning.assert_called_once_with(
+            "GITHUB_COPILOT_API_KEY_URL is no longer used; LiteLLM sends the OAuth access token directly"
+        )
+
     def test_get_github_headers(self, authenticator):
         headers = authenticator._get_github_headers()
         assert headers == {