diff --git a/litellm/proxy/auth/v2/authenticators.py b/litellm/proxy/auth/v2/authenticators.py
index 2e305555852..5dea06b0ef4 100644
--- a/litellm/proxy/auth/v2/authenticators.py
+++ b/litellm/proxy/auth/v2/authenticators.py
@@ -101,15 +101,28 @@ def _load_jwt_settings() -> Any:
     )
 
 
+def _jwt_is_configured() -> bool:
+    import os
+
+    from litellm.proxy.proxy_server import general_settings
+
+    cfg = (general_settings or {}).get("auth_v2_jwt") or {}
+    return bool(cfg.get("jwks_uri") or os.getenv("AUTH_V2_JWKS_URI"))
+
+
 class JWTAuthenticator:
     """Verifies a bearer JWT with authlib and maps its claims to an identity."""
 
     def can_handle(self, api_key: Optional[str]) -> bool:
-        return (
+        # Only claim JWT-shaped tokens when JWT auth is actually configured, so an
+        # unconfigured deployment falls through to a clean 401 instead of a 500.
+        if not (
             isinstance(api_key, str)
             and not api_key.startswith("sk-")
             and api_key.count(".") == 2
-        )
+        ):
+            return False
+        return _jwt_is_configured()
 
     async def authenticate(self, api_key: str, ctx: AuthContext) -> Any:
         from litellm.proxy._types import LitellmUserRoles, UserAPIKeyAuth
diff --git a/tests/test_litellm/proxy/auth/v2/test_authenticators.py b/tests/test_litellm/proxy/auth/v2/test_authenticators.py
index 4747dde5296..45401cc534d 100644
--- a/tests/test_litellm/proxy/auth/v2/test_authenticators.py
+++ b/tests/test_litellm/proxy/auth/v2/test_authenticators.py
@@ -1,10 +1,13 @@
 import pytest
 
 from litellm.proxy.auth.v2.authenticators import (
+    JWTAuthenticator,
     MasterKeyAuthenticator,
     VirtualKeyAuthenticator,
 )
 
+JWT_SHAPED = "header.payload.signature"
+
 MASTER = "sk-master-secret-123"
 
 
@@ -40,3 +43,27 @@ def test_virtual_key_handles_sk_prefix_but_not_master_first():
     assert vk.can_handle("sk-abc123") is True
     assert vk.can_handle("not-a-key") is False
     assert vk.can_handle(None) is False
+
+
+def test_jwt_authenticator_inert_when_unconfigured(monkeypatch):
+    # No auth_v2_jwt config and no env var: a JWT-shaped token must fall through
+    # (can_handle False) so the chain ends in a clean 401, not a 500.
+    monkeypatch.setattr(
+        "litellm.proxy.proxy_server.general_settings", {}, raising=False
+    )
+    monkeypatch.delenv("AUTH_V2_JWKS_URI", raising=False)
+    assert JWTAuthenticator().can_handle(JWT_SHAPED) is False
+
+
+def test_jwt_authenticator_handles_jwt_shape_when_configured(monkeypatch):
+    monkeypatch.setattr(
+        "litellm.proxy.proxy_server.general_settings",
+        {"auth_v2_jwt": {"jwks_uri": "https://idp.example/jwks"}},
+        raising=False,
+    )
+    auth = JWTAuthenticator()
+    assert auth.can_handle(JWT_SHAPED) is True
+    # Still only claims JWT-shaped tokens, never virtual keys or non-3-part values.
+    assert auth.can_handle("sk-abc.def.ghi") is False
+    assert auth.can_handle("not.a.jwt.token") is False
+    assert auth.can_handle(None) is False