diff --git a/tests/entrypoints/openai/responses/test_serving_responses.py b/tests/entrypoints/openai/responses/test_serving_responses.py
index 1a315902e2..429fcf1d0d 100644
--- a/tests/entrypoints/openai/responses/test_serving_responses.py
+++ b/tests/entrypoints/openai/responses/test_serving_responses.py
@@ -748,6 +748,7 @@ class TestInitializeToolSessions:
         class ToolCallingHarmonyContext(HarmonyContext):
             def __init__(self):
                 self._messages = []
+                self.request = None
                 self._needs_tool_call = True
 
             def append_output(self, output) -> None:
@@ -804,6 +805,53 @@ class TestInitializeToolSessions:
         assert followup_engine_input.get("cache_salt") == "request-salt"
         assert followup_engine_input["prompt_token_ids"] == [3, 4]
 
+    @pytest.mark.asyncio
+    async def test_harmony_tool_followup_respects_max_output_tokens(
+        self, serving_responses_instance
+    ):
+        class ToolCallingHarmonyContext(HarmonyContext):
+            def __init__(self, request):
+                self._messages = []
+                self.request = request
+                self._needs_tool_call = True
+
+            def append_output(self, output) -> None:
+                pass
+
+            def need_builtin_tool_call(self) -> bool:
+                return self._needs_tool_call
+
+            async def call_tool(self):
+                self._needs_tool_call = False
+                return []
+
+            def append_tool_output(self, output) -> None:
+                pass
+
+        max_tokens_per_turn = []
+
+        async def generate_output(engine_input, sampling_params, *args, **kwargs):
+            max_tokens_per_turn.append(sampling_params.max_tokens)
+            yield MagicMock()
+
+        serving_responses_instance.engine_client.generate.side_effect = generate_output
+        serving_responses_instance.online_renderer.render_responses_harmony_messages = (
+            MagicMock(return_value=tokens_input([1, 2, 3]))
+        )
+        context = ToolCallingHarmonyContext(
+            ResponsesRequest(input="test", max_output_tokens=10)
+        )
+
+        async for _ in serving_responses_instance._generate_with_builtin_tools(
+            request_id="req",
+            engine_input=tokens_input([1]),
+            sampling_params=SamplingParams(max_tokens=10),
+            context=context,
+        ):
+            pass
+
+        assert max_tokens_per_turn == [10, 10]
+
     @pytest.mark.asyncio
     async def test_initialize_tool_sessions(
         self, serving_responses_instance, mock_context, mock_exit_stack
diff --git a/vllm/entrypoints/openai/responses/context.py b/vllm/entrypoints/openai/responses/context.py
index 0db47cf367..59b42f96a3 100644
--- a/vllm/entrypoints/openai/responses/context.py
+++ b/vllm/entrypoints/openai/responses/context.py
@@ -615,12 +615,14 @@ class HarmonyContext(ConversationContext):
         available_tools: list[str],
         function_tool_names: frozenset[str],
         response_parser: Parser | None = None,
+        request: ResponsesRequest | None = None,
     ):
         from vllm.parser.harmony import HarmonyParser, Segment
 
         assert isinstance(response_parser, HarmonyParser)
 
         self._messages = messages
+        self.request = request
         self.response_parser: HarmonyParser = response_parser
         self.finish_reason: str | None = None
         self.available_tools = available_tools
diff --git a/vllm/entrypoints/openai/responses/serving.py b/vllm/entrypoints/openai/responses/serving.py
index 8108c5f775..9fba86b80c 100644
--- a/vllm/entrypoints/openai/responses/serving.py
+++ b/vllm/entrypoints/openai/responses/serving.py
@@ -443,6 +443,7 @@ class OpenAIServingResponses(GenerateBaseServing):
                     available_tools,
                     function_tool_names,
                     response_parser=response_parser,
+                    request=request,
                 )
             else:
                 if envs.VLLM_USE_EXPERIMENTAL_PARSER_CONTEXT:
@@ -678,8 +679,12 @@ class OpenAIServingResponses(GenerateBaseServing):
                     tok_params=tok_params,
                 )
 
-                sampling_params.max_tokens = max_model_len - self._extract_prompt_len(
-                    engine_input
+                sampling_params.max_tokens = get_max_tokens(
+                    max_model_len,
+                    context.request.max_output_tokens if context.request else None,
+                    self._extract_prompt_len(engine_input),
+                    self.default_sampling_params,
+                    self.override_max_tokens,
                 )
             elif isinstance(context, ParsableContext):
                 (engine_input,) = await self._render_next_turn(