diff --git a/hermes_cli/copilot_auth.py b/hermes_cli/copilot_auth.py
index d520b1310b..ce7c0dd117 100644
--- a/hermes_cli/copilot_auth.py
+++ b/hermes_cli/copilot_auth.py
@@ -25,7 +25,10 @@ logger = logging.getLogger(__name__)
 # VS Code's GitHub App client ID: mints ghu_* tokens exchangeable for Copilot API JWTs (needed for
 # internal-only models / enterprise endpoints). The opencode App ID mints gho_* tokens that 404.
 COPILOT_OAUTH_CLIENT_ID = "Iv1.b507a08c87ecfe98"
-_CLASSIC_PAT_PREFIX = "ghp_"  # rejected by the Copilot API (gho_ / github_pat_ / ghu_ work)
+_CLASSIC_PAT_PREFIX = "ghp_"  # rejected by the Copilot API
+# Token families the Copilot API exchanges. Anything else (a random string in GITHUB_TOKEN) used
+# to pass validation and then fail downstream with an opaque auth error (#12650).
+_SUPPORTED_PREFIXES = ("gho_", "github_pat_", "ghu_")
 COPILOT_ENV_VARS = ("COPILOT_GITHUB_TOKEN", "GH_TOKEN", "GITHUB_TOKEN")
 _DEVICE_CODE_POLL_INTERVAL = 5  # seconds
 _DEVICE_CODE_POLL_SAFETY_MARGIN = 3  # seconds
@@ -43,6 +46,10 @@ def validate_copilot_token(token: str) -> tuple[bool, str]:
             "  → `copilot login` or `hermes model` to authenticate via OAuth\n"
             "  → A fine-grained PAT (github_pat_*) with Copilot Requests permission\n"
             "  → `gh auth login` with the default device code flow (produces gho_* tokens)")
+    if not token.startswith(_SUPPORTED_PREFIXES):
+        return False, (
+            "Unsupported GitHub token format for the Copilot API. "
+            f"Supported token prefixes: {', '.join(_SUPPORTED_PREFIXES)}.")
     return True, "OK"
 
 
@@ -73,7 +80,7 @@ def resolve_copilot_token() -> tuple[str, str]:
     if token:
         valid, msg = validate_copilot_token(token)
         if not valid:
-            raise ValueError(f"Token from `gh auth token` is a classic PAT (ghp_*). {msg}")
+            raise ValueError(f"Token from `gh auth token` is not usable with Copilot. {msg}")
         return token, "gh auth token"
     return "", ""
 
diff --git a/tests/hermes_cli/test_copilot_auth.py b/tests/hermes_cli/test_copilot_auth.py
index 334f1eb2e4..a8c20ac6ec 100644
--- a/tests/hermes_cli/test_copilot_auth.py
+++ b/tests/hermes_cli/test_copilot_auth.py
@@ -14,6 +14,18 @@ class TestTokenValidation:
         assert "Classic Personal Access Tokens" in msg
         assert "ghp_" in msg
 
+    @pytest.mark.parametrize("token", ["gho_abcdefghijklmnop1234", "github_pat_abcdefghijklmnop1234", "ghu_abcdefghijklmnop1234"])
+    def test_supported_token_families_accepted(self, token):
+        from hermes_cli.copilot_auth import validate_copilot_token
+        assert validate_copilot_token(token) == (True, "OK")
+
+    def test_arbitrary_string_rejected(self):
+        """A non-GitHub value in GITHUB_TOKEN must fail validation instead of reaching the API (#12650)."""
+        from hermes_cli.copilot_auth import validate_copilot_token
+        valid, msg = validate_copilot_token("not_a_github_token")
+        assert valid is False
+        assert "Supported token prefixes" in msg
+
 
 class TestResolveToken:
     """Token resolution with env var priority."""
@@ -37,7 +49,7 @@ class TestResolveToken:
         monkeypatch.delenv("GH_TOKEN", raising=False)
         monkeypatch.delenv("GITHUB_TOKEN", raising=False)
         with patch("hermes_cli.copilot_auth._try_gh_cli_token", return_value="ghp_classic"):
-            with pytest.raises(ValueError, match="classic PAT"):
+            with pytest.raises(ValueError, match="Classic Personal Access Tokens"):
                 resolve_copilot_token()
 
     def test_invalid_env_var_skips_gh_cli_fallback(self, monkeypatch):