diff --git a/litellm/proxy/auth/user_api_key_auth.py b/litellm/proxy/auth/user_api_key_auth.py
index 526a47b1b98..d28e1209f4e 100644
--- a/litellm/proxy/auth/user_api_key_auth.py
+++ b/litellm/proxy/auth/user_api_key_auth.py
@@ -602,6 +602,15 @@ async def check_api_key_for_custom_headers_or_pass_through_endpoints(
     return api_key
 
 
+# Cache sentinel written when a JWT under AUTO_REGISTER resolved to a proxy
+# admin via auth_builder. Proxy admins don't need a mapped virtual key (they
+# have full access via auth_builder anyway), but without a cache entry every
+# subsequent request from the same JWT identity would re-query the DB for a
+# non-existent mapping. Sentinel tells _resolve_jwt_to_virtual_key to skip
+# the lookup and return None (caller proceeds to auth_builder).
+_JWT_PROXY_ADMIN_SENTINEL = "__JWT_PROXY_ADMIN__"
+
+
 class _PendingAutoRegister(NamedTuple):
     """
     Signal returned by ``_resolve_jwt_to_virtual_key`` when the JWT's claim is
@@ -808,6 +817,12 @@ async def _resolve_jwt_to_virtual_key(
     cache_key = f"jwt_key_mapping:{virtual_key_claim_field}:{claim_value}"
     cached_mapping = await user_api_key_cache.async_get_cache(cache_key)
 
+    if cached_mapping == _JWT_PROXY_ADMIN_SENTINEL:
+        # Previously resolved to a proxy admin via auth_builder; skip the
+        # mapping lookup and let the caller re-run auth_builder. Avoids a
+        # repeated DB hit on every proxy-admin request under AUTO_REGISTER.
+        return None
+
     if cached_mapping == "__NO_MAPPING__":
         behavior = jwt_handler.litellm_jwtauth.unregistered_jwt_client_behavior
         if behavior == UnregisteredJWTClientBehavior.REJECT:
@@ -1159,6 +1174,19 @@ async def _user_api_key_auth_builder(  # noqa: PLR0915
                     jwt_claims = result.get("jwt_claims", None)
 
                     if is_proxy_admin:
+                        # Proxy admins authenticate via auth_builder (full
+                        # access), not via a mapped virtual key. If
+                        # AUTO_REGISTER was pending, cache a sentinel so
+                        # future requests from this JWT identity skip the
+                        # DB mapping lookup in _resolve_jwt_to_virtual_key.
+                        # Without this, every proxy-admin request under
+                        # AUTO_REGISTER re-hits get_jwt_key_mapping_object.
+                        if pending_auto_register is not None:
+                            await user_api_key_cache.async_set_cache(
+                                key=pending_auto_register.cache_key,
+                                value=_JWT_PROXY_ADMIN_SENTINEL,
+                                ttl=jwt_handler.litellm_jwtauth.virtual_key_mapping_cache_ttl,
+                            )
                         return UserAPIKeyAuth(
                             api_key=None,
                             user_role=LitellmUserRoles.PROXY_ADMIN,
diff --git a/tests/proxy_unit_tests/test_jwt_key_mapping.py b/tests/proxy_unit_tests/test_jwt_key_mapping.py
index 15c3834d1a6..4ad7095a9aa 100644
--- a/tests/proxy_unit_tests/test_jwt_key_mapping.py
+++ b/tests/proxy_unit_tests/test_jwt_key_mapping.py
@@ -27,7 +27,6 @@ from litellm.proxy.management_endpoints.jwt_key_mapping_endpoints import (
 from litellm.caching.caching import DualCache
 from fastapi import HTTPException
 
-
 # ──────────────────────────────────────────────
 # Tests: _resolve_jwt_to_virtual_key
 # ──────────────────────────────────────────────
@@ -1174,6 +1173,51 @@ async def test_auto_register_raises_503_when_winner_mapping_vanishes():
     assert "concurrently removed" in exc_info.value.detail
 
 
+@pytest.mark.asyncio
+async def test_proxy_admin_sentinel_skips_db_lookup_on_cache_hit():
+    """
+    When the cache holds the proxy-admin sentinel (written after a prior
+    request's is_proxy_admin early-return), _resolve_jwt_to_virtual_key must
+    return None *without* hitting the DB. Caller proceeds to auth_builder.
+
+    Without this, every subsequent proxy-admin request under AUTO_REGISTER
+    would re-query get_jwt_key_mapping_object — a cache-miss regression
+    introduced by the deferred-auto-register refactor.
+    """
+    from litellm.proxy._types import UnregisteredJWTClientBehavior
+
+    jwt_handler = JWTHandler()
+    jwt_handler.litellm_jwtauth = LiteLLM_JWTAuth(
+        virtual_key_claim_field="sub",
+        unregistered_jwt_client_behavior=UnregisteredJWTClientBehavior.AUTO_REGISTER,
+        virtual_key_mapping_cache_ttl=300,
+    )
+    jwt_claims = {"sub": "admin-user"}
+
+    prisma_client = MagicMock()
+    # Will fail the test if accessed — proves the sentinel short-circuits DB
+    prisma_client.db.litellm_jwtkeymapping.find_first = AsyncMock(
+        side_effect=AssertionError("DB must not be hit when sentinel is cached")
+    )
+
+    user_api_key_cache = DualCache()
+    await user_api_key_cache.async_set_cache(
+        "jwt_key_mapping:sub:admin-user", "__JWT_PROXY_ADMIN__"
+    )
+
+    result = await _resolve_jwt_to_virtual_key(
+        jwt_claims=jwt_claims,
+        jwt_handler=jwt_handler,
+        prisma_client=prisma_client,
+        user_api_key_cache=user_api_key_cache,
+        parent_otel_span=None,
+        proxy_logging_obj=None,
+    )
+
+    assert result is None
+    prisma_client.db.litellm_jwtkeymapping.find_first.assert_not_called()
+
+
 # ──────────────────────────────────────────────
 # Tests: AUTO_REGISTER stamps validated identity from auth_builder
 # ──────────────────────────────────────────────