diff --git a/litellm/router_strategy/auto_router/auto_router.py b/litellm/router_strategy/auto_router/auto_router.py
index 20c0ece46b6..86383a27880 100644
--- a/litellm/router_strategy/auto_router/auto_router.py
+++ b/litellm/router_strategy/auto_router/auto_router.py
@@ -128,13 +128,14 @@ class AutoRouter(CustomLogger):
         """
         from semantic_router.routers import SemanticRouter
 
+        from litellm.litellm_core_utils.prompt_templates.factory import resolve_structured_messages
         from litellm.router_strategy.auto_router.litellm_encoder import (
             LiteLLMRouterEncoder,
         )
         from litellm.types.router import PreRoutingHookResponse
 
-        if messages is None:
-            # do nothing, return same inputs
+        resolved_messages: Final = resolve_structured_messages(messages=messages, request_kwargs=request_kwargs)
+        if resolved_messages is None:
             return None
 
         routelayer = self.routelayer
@@ -153,7 +154,7 @@ class AutoRouter(CustomLogger):
             )
             self.routelayer = routelayer
 
-        message_content: Final = self._extract_text_from_messages(messages)
+        message_content: Final = self._extract_text_from_messages(resolved_messages)
         route_name: Final = self._matched_route_name(routelayer, message_content)
 
         return PreRoutingHookResponse(
diff --git a/tests/test_litellm/router_strategy/test_auto_router.py b/tests/test_litellm/router_strategy/test_auto_router.py
index b73485e6019..10d133e7311 100644
--- a/tests/test_litellm/router_strategy/test_auto_router.py
+++ b/tests/test_litellm/router_strategy/test_auto_router.py
@@ -479,3 +479,70 @@ class TestAutoRouterEmbeddingInputCap:
 
         assert auto_router.routelayer is not None
         assert auto_router.routelayer.encoder.max_input_chars == 777
+
+
+class TestAutoRouterRoutesResponsesApiInput:
+    """Responses API requests carry the prompt in `input`, not `messages`, and still have to reach the route layer."""
+
+    @pytest.mark.asyncio
+    async def test_should_route_a_string_input_when_messages_is_none(self):
+        from semantic_router.schema import RouteChoice
+
+        layer: Final = FixedRouteLayer(RouteChoice(name="code-model"))
+        auto_router: Final = _auto_router(layer)
+
+        result: Final = await auto_router.async_pre_routing_hook(
+            model="my-auto-router",
+            request_kwargs={
+                "input": "fix this stack trace",
+                "litellm_metadata": {"user_api_key_request_route": "/v1/responses"},
+            },
+            messages=None,
+        )
+
+        assert result is not None
+        assert result.model == "code-model"
+        assert result.messages is None
+        assert layer.seen_text == "fix this stack trace"
+
+    @pytest.mark.asyncio
+    async def test_should_route_a_list_input_with_instructions_when_messages_is_none(self):
+        from semantic_router.schema import RouteChoice
+
+        layer: Final = FixedRouteLayer(RouteChoice(name="code-model"))
+        auto_router: Final = _auto_router(layer)
+
+        result: Final = await auto_router.async_pre_routing_hook(
+            model="my-auto-router",
+            request_kwargs={
+                "instructions": "You are a coding agent.",
+                "input": [
+                    {
+                        "type": "message",
+                        "role": "user",
+                        "content": [{"type": "input_text", "text": "fix this stack trace"}],
+                    }
+                ],
+                "litellm_metadata": {"user_api_key_request_route": "/v1/responses"},
+            },
+            messages=None,
+        )
+
+        assert result is not None
+        assert result.model == "code-model"
+        assert layer.seen_text is not None
+        assert "fix this stack trace" in layer.seen_text
+
+    @pytest.mark.asyncio
+    async def test_should_skip_routing_when_neither_messages_nor_input_is_present(self):
+        layer: Final = FixedRouteLayer(None)
+        auto_router: Final = _auto_router(layer)
+
+        result: Final = await auto_router.async_pre_routing_hook(
+            model="my-auto-router",
+            request_kwargs={"litellm_metadata": {"user_api_key_request_route": "/v1/responses"}},
+            messages=None,
+        )
+
+        assert result is None
+        assert layer.seen_text is None