diff --git a/litellm/proxy/_types.py b/litellm/proxy/_types.py
index 1621eb4dd65..29bdc350446 100644
--- a/litellm/proxy/_types.py
+++ b/litellm/proxy/_types.py
@@ -5303,8 +5303,9 @@ class LiteLLM_JWTAuth(LiteLLMPydanticObjectBase):
         description=(
             "Only used with unregistered_jwt_client_behavior='auto_register'. When True, the JWT claim is "
             "mapped to a virtual key the resolved internal user already owns instead of minting a new one. "
-            "If the user owns several, the most recently created non-expired key is chosen. A new key is "
-            "only minted when the user has none."
+            "If the user owns several, the most recently created key that can call LLM routes is chosen: "
+            "not blocked, not expired, not an Admin UI session key, and with no route restriction other than "
+            "llm_api_routes. A new key is only minted when the user has no such key."
         ),
     )
     routing_overrides: list[JWTRoutingOverride] | None = Field(
diff --git a/litellm/proxy/auth/user_api_key_auth.py b/litellm/proxy/auth/user_api_key_auth.py
index 59b92f84b52..f537f048d1e 100644
--- a/litellm/proxy/auth/user_api_key_auth.py
+++ b/litellm/proxy/auth/user_api_key_auth.py
@@ -931,7 +931,7 @@ class _PendingAutoRegister(NamedTuple):
 
 
 async def _latest_active_key_hash_for_user(prisma_client: PrismaClient, user_id: str) -> str | None:
-    row: Final = await VerificationTokenRepository(prisma_client).find_latest_active_row_by_user_id(user_id)
+    row: Final = await VerificationTokenRepository(prisma_client).find_latest_llm_api_row_by_user_id(user_id)
     return None if row is None else row.token
 
 
diff --git a/litellm/repositories/verification_token_repository.py b/litellm/repositories/verification_token_repository.py
index 63f0bb030d9..a01737cfd1e 100644
--- a/litellm/repositories/verification_token_repository.py
+++ b/litellm/repositories/verification_token_repository.py
@@ -8,6 +8,7 @@ from datetime import datetime, timezone
 from types import TracebackType
 from typing import TYPE_CHECKING, Final, Protocol
 
+from litellm.constants import UI_SESSION_TOKEN_TEAM_ID
 from litellm.models.verification_token import (
     LiteLLM_VerificationToken,
 )
@@ -123,8 +124,7 @@ class VerificationTokenRepository(BaseRepository[LiteLLM_VerificationToken]):
         records: Final[Sequence[PrismaVerificationToken]] = await self.table.find_many(where={"user_id": user_id})
         return self._to_model_list(records)
 
-    async def find_latest_active_row_by_user_id(self, user_id: str) -> "PrismaVerificationToken | None":
-        """Find the most recently created non-blocked, non-expired token row for a user."""
+    async def find_latest_llm_api_row_by_user_id(self, user_id: str) -> "PrismaVerificationToken | None":
         row: Final = await self.table.find_first(
             where={  # mutable-ok: the prisma where clause contract is a plain dict
                 "user_id": user_id,
@@ -136,6 +136,18 @@ class VerificationTokenRepository(BaseRepository[LiteLLM_VerificationToken]):
                             {"expires": {"gt": datetime.now(timezone.utc)}},  # mutable-ok: prisma filter literal
                         ]
                     },
+                    {  # mutable-ok: prisma filter literal
+                        "OR": [  # mutable-ok: prisma filter literal
+                            {"team_id": None},  # mutable-ok: prisma filter literal
+                            {"team_id": {"not": UI_SESSION_TOKEN_TEAM_ID}},  # mutable-ok: prisma filter literal
+                        ]
+                    },
+                    {  # mutable-ok: prisma filter literal
+                        "OR": [  # mutable-ok: prisma filter literal
+                            {"allowed_routes": {"is_empty": True}},  # mutable-ok: prisma filter literal
+                            {"allowed_routes": {"has": "llm_api_routes"}},  # mutable-ok: prisma filter literal
+                        ]
+                    },
                 ],
             },
             order={"created_at": "desc"},  # mutable-ok: prisma order literal
diff --git a/tests/test_litellm/proxy/auth/test_user_api_key_auth.py b/tests/test_litellm/proxy/auth/test_user_api_key_auth.py
index c8215bf15e0..a012e5b20b4 100644
--- a/tests/test_litellm/proxy/auth/test_user_api_key_auth.py
+++ b/tests/test_litellm/proxy/auth/test_user_api_key_auth.py
@@ -2199,6 +2199,43 @@ async def test_auto_register_map_existing_key_reuses_users_latest_key():
     assert result.org_id == "key-own-org"
 
 
+@pytest.mark.asyncio
+async def test_auto_register_map_existing_key_skips_keys_that_cannot_call_llm_routes():
+    from typing import Final
+
+    from litellm.constants import UI_SESSION_TOKEN_TEAM_ID
+    from litellm.proxy.auth.user_api_key_auth import _auto_register_jwt_mapping
+
+    prisma_client = MagicMock()
+    prisma_client.db.litellm_verificationtoken.find_first = AsyncMock(
+        return_value=SimpleNamespace(token="existing-hash")
+    )
+    prisma_client.db.litellm_jwtkeymapping.create = AsyncMock()
+
+    user_api_key_cache = MagicMock()
+    user_api_key_cache.async_set_cache = AsyncMock()
+
+    jwt_handler = MagicMock()
+    jwt_handler.litellm_jwtauth = LiteLLM_JWTAuth(
+        auto_register_map_existing_key=True,
+        virtual_key_mapping_cache_ttl=300,
+    )
+
+    generate_patch, resolve_patch = _auto_register_patches(plaintext_key=None)
+    with generate_patch, resolve_patch:
+        await _auto_register_jwt_mapping(**_auto_register_kwargs(prisma_client, user_api_key_cache, jwt_handler))
+
+    where = prisma_client.db.litellm_verificationtoken.find_first.await_args.kwargs["where"]
+    team_or: Final = next(entry["OR"] for entry in where["AND"] if any("team_id" in e for e in entry["OR"]))
+    assert {"team_id": {"not": UI_SESSION_TOKEN_TEAM_ID}} in team_or, f"UI session keys must be excluded: {where}"
+    assert {"team_id": None} in team_or, f"keys without a team must stay eligible: {where}"
+    routes_or: Final = next(entry["OR"] for entry in where["AND"] if any("allowed_routes" in e for e in entry["OR"]))
+    assert routes_or == [
+        {"allowed_routes": {"is_empty": True}},
+        {"allowed_routes": {"has": "llm_api_routes"}},
+    ], f"only unrestricted or llm_api_routes keys may be reused: {where}"
+
+
 @pytest.mark.asyncio
 async def test_auto_register_map_existing_key_mints_when_user_has_no_key():
     """The flag must not leave a keyless user unmapped: with no existing key it