diff --git a/nemo_rl/models/generation/vllm/vllm_worker_async.py b/nemo_rl/models/generation/vllm/vllm_worker_async.py
index e791fa4a02..439fb93f48 100644
--- a/nemo_rl/models/generation/vllm/vllm_worker_async.py
+++ b/nemo_rl/models/generation/vllm/vllm_worker_async.py
@@ -440,10 +440,12 @@ def _clamp_max_tokens(
                 """Clamp the request's max output tokens so that input + output <= max_model_len."""
                 remaining = self.model_config.max_model_len - len(prompt_token_ids)
                 if remaining <= 0:
-                    raise ValueError(
+                    # preserve the literal "context length" in this message to match Gym's overflow handling
+                    raise VLLMValidationError(
                         f"Prompt length ({len(prompt_token_ids)}) fills or exceeds "
-                        f"max_model_len ({self.model_config.max_model_len}). "
-                        f"No room for output tokens."
+                        f"this model's maximum context length ({self.model_config.max_model_len}). "
+                        f"No room for output tokens.",
+                        parameter="max_model_len",
                     )
                 max_tokens = min(request_max_tokens, remaining)
                 self._set_max_tokens(request, max_tokens)
diff --git a/tests/unit/models/generation/test_vllm_generation.py b/tests/unit/models/generation/test_vllm_generation.py
index b15c4a21fa..9b9de7ec93 100644
--- a/tests/unit/models/generation/test_vllm_generation.py
+++ b/tests/unit/models/generation/test_vllm_generation.py
@@ -289,7 +289,9 @@ def __init__(self, **kwargs):
             self.instances.append(self)
 
     class VLLMValidationError(Exception):
-        pass
+        def __init__(self, message="", parameter=None):
+            super().__init__(message)
+            self.parameter = parameter
 
     class ToolParserManager:
         import_tool_parser = MagicMock()
@@ -401,6 +403,72 @@ def test_vllm_async_http_server_loads_reasoning_parser_plugin(monkeypatch):
     assert "reasoning_parser_plugin" not in openai_serving_chat.instances[0].kwargs
 
 
+def _nemo_gym_recognizes_context_overflow(
+    *, status: int, response_content: str
+) -> bool:
+    """Mirror responses_api_models/vllm_model/app.py overflow detection."""
+    return status == 400 and (
+        "context length" in response_content or "max_tokens" in response_content
+    )
+
+
+@pytest.mark.asyncio
+async def test_vllm_http_server_context_overflow_matches_nemo_gym(monkeypatch):
+    """Overflow from _clamp_max_tokens must be HTTP 400 that NeMo Gym recognizes."""
+    _, _, openai_serving_chat = _install_fake_vllm_openai_modules(monkeypatch)
+
+    worker = VllmAsyncGenerationWorkerImpl.__new__(VllmAsyncGenerationWorkerImpl)
+    worker.cfg = {
+        "temperature": 1.0,
+        "top_p": 1.0,
+        "val_temperature": 0.0,
+        "val_top_p": 1.0,
+        "vllm_cfg": {},
+    }
+    worker.llm = MagicMock(model_config="model-config", renderer="renderer")
+    worker.llm_async_engine_args = MagicMock()
+    worker.llm_async_engine_args.create_model_config.return_value = MagicMock(
+        served_model_name="served-model", model="model-path"
+    )
+
+    app = _FakeFastAPIApp()
+    worker._setup_vllm_openai_api_server(app)
+
+    max_model_len = 128
+    renderer = openai_serving_chat.instances[0].kwargs["online_renderer"]
+    renderer.model_config = types.SimpleNamespace(max_model_len=max_model_len)
+    serving_chat = openai_serving_chat.instances[0]
+    chat_handler = next(
+        handler for path, handler in app.routes if path == "/v1/chat/completions"
+    )
+    overflow_prompt = [0] * max_model_len
+
+    async def create_chat_completion(request, _raw_request):
+        renderer._clamp_max_tokens(request, request.max_tokens, overflow_prompt)
+
+    serving_chat.create_chat_completion = create_chat_completion
+    response = await chat_handler(
+        types.SimpleNamespace(
+            top_k=-1,
+            top_p=1.0,
+            temperature=1.0,
+            max_tokens=1,
+            max_completion_tokens=None,
+        ),
+        MagicMock(),
+    )
+
+    response_content = response.body.decode()
+    assert response.status_code == 400
+    assert _nemo_gym_recognizes_context_overflow(
+        status=response.status_code,
+        response_content=response_content,
+    )
+    error = json.loads(response_content)["error"]
+    assert error["type"] == "invalid_request_error"
+    assert error["code"] == 400
+
+
 def test_nano_v3_reasoning_parser_swaps_reasoning_when_thinking_disabled(
     monkeypatch,
 ):