diff --git a/agents/vanilla_python/templates/openai_responses_agent/src/openai_responses_agent/agent.py b/agents/vanilla_python/templates/openai_responses_agent/src/openai_responses_agent/agent.py
index 21567f77..04739c3a 100644
--- a/agents/vanilla_python/templates/openai_responses_agent/src/openai_responses_agent/agent.py
+++ b/agents/vanilla_python/templates/openai_responses_agent/src/openai_responses_agent/agent.py
@@ -130,7 +130,13 @@ def _messages_to_responses_input(
 
 
 def _get_output_text_from_response(response: Any) -> str:
-    """Extract assistant text from Responses API response (response.output[].content[])."""
+    """Extract assistant text from a Responses API or Chat Completions API response."""
+    # Chat Completions format: response.choices[0].message.content
+    choices = getattr(response, "choices", None)
+    if choices:
+        return getattr(choices[0].message, "content", None) or ""
+
+    # Responses API format: response.output[].content[]
     if not getattr(response, "output", None) or not response.output:
         return ""
     for item in response.output:
@@ -186,6 +192,7 @@ def __init__(
         self.temperature = temperature
         self.tools: dict[str, Callable] = {}
         self.messages: list[dict[str, Any]] = []
+        self._use_responses_api: bool | None = None
         self.action_re = re.compile(r"Action:\s*(\w+)\s*\((.*?)\)")
 
     def add_message(self, role: str, content: str) -> None:
@@ -206,14 +213,49 @@ def _parse_arguments(self, args_str: str) -> list[str]:
         args = next(reader, [])
         return [arg.strip().strip("'\"") for arg in args]
 
-    def _responses_create(
+    def _chat_completions_create(
+        self,
+        messages: list[dict[str, Any]] | None = None,
+        temperature: float | None = None,
+        model: str | None = None,
+    ) -> Any:
+        """
+        Single Chat Completions API call via OpenAI client.
+
+        Args:
+            messages: List of messages; if None, self.messages is used.
+            temperature: Override temperature for this call.
+            model: Override model for this call.
+
+        Returns:
+            Response from client.chat.completions.create.
+        """
+        msg_list = messages if messages is not None else self.messages
+        temp = temperature if temperature is not None else self.temperature
+        model_id = model if model is not None else self.model
+
+        kwargs: dict[str, Any] = {
+            "model": model_id,
+            "messages": msg_list,
+        }
+        if temp is not None:
+            kwargs["temperature"] = temp
+
+        return self.client.chat.completions.create(**kwargs)
+
+    def _llm_create(
         self,
         messages: list[dict[str, Any]] | None = None,
         temperature: float | None = None,
         model: str | None = None,
     ) -> Any:
         """
-        Single Responses API call via OpenAI client.
+        LLM API call with automatic fallback from Responses API to Chat Completions.
+
+        Tries the Responses API unless a prior 404 permanently disabled it. If the
+        server returns HTTP 404, permanently falls back to Chat Completions for all
+        subsequent calls. On HTTP 400, falls back for the current call only (400 can
+        also indicate a legitimate request error, not just an unsupported endpoint).
 
         Args:
             messages: List of messages; if None, self.messages is used.
@@ -221,8 +263,14 @@ def _responses_create(
             model: Override model for this call.
 
         Returns:
-            Response from client.responses.create (object with .output etc.).
+            Response from the Responses API or Chat Completions API.
         """
+        # Fast path: already know which API to use
+        if self._use_responses_api is False:
+            return self._chat_completions_create(
+                messages=messages, temperature=temperature, model=model
+            )
+
         msg_list = messages if messages is not None else self.messages
         temp = temperature if temperature is not None else self.temperature
         model_id = model if model is not None else self.model
@@ -233,14 +281,36 @@ def _responses_create(
             "instructions": instructions,
             "input": input_items,
         }
-        if temp != 0:
+        if temp is not None:
             kwargs["temperature"] = temp
 
-        return self.client.responses.create(**kwargs)
+        try:
+            response = self.client.responses.create(**kwargs)
+            if self._use_responses_api is None:
+                self._use_responses_api = True
+                logger.info("Using Responses API (supported by server)")
+            return response
+        except APIStatusError as exc:
+            if exc.status_code not in (400, 404):
+                raise
+            if exc.status_code == 404:
+                self._use_responses_api = False
+                logger.info(
+                    "Responses API not found (HTTP 404), "
+                    "permanently falling back to Chat Completions API",
+                )
+            else:
+                logger.info(
+                    "Responses API returned HTTP 400, "
+                    "falling back to Chat Completions API for this call",
+                )
+            return self._chat_completions_create(
+                messages=messages, temperature=temperature, model=model
+            )
 
     def _execute(self) -> str:
-        """Execute a Responses API request."""
-        response = self._responses_create(
+        """Execute an LLM API request (Responses API with Chat Completions fallback)."""
+        response = self._llm_create(
             messages=self.messages,
             temperature=self.temperature,
             model=self.model,
diff --git a/agents/vanilla_python/templates/openai_responses_agent/tests/test_agent.py b/agents/vanilla_python/templates/openai_responses_agent/tests/test_agent.py
new file mode 100644
index 00000000..20323c3b
--- /dev/null
+++ b/agents/vanilla_python/templates/openai_responses_agent/tests/test_agent.py
@@ -0,0 +1,174 @@
+from types import SimpleNamespace
+from unittest.mock import MagicMock, patch
+
+import pytest
+from openai import APIStatusError
+from openai_responses_agent.agent import AIAgent, _get_output_text_from_response
+
+
+class TestGetOutputTextFromResponse:
+    def test_chat_completions_format(self):
+        response = SimpleNamespace(
+            choices=[SimpleNamespace(message=SimpleNamespace(content="hello"))]
+        )
+        assert _get_output_text_from_response(response) == "hello"
+
+    def test_chat_completions_none_content(self):
+        response = SimpleNamespace(
+            choices=[SimpleNamespace(message=SimpleNamespace(content=None))]
+        )
+        assert _get_output_text_from_response(response) == ""
+
+    def test_responses_api_format(self):
+        block = SimpleNamespace(type="output_text", text="world")
+        item = SimpleNamespace(content=[block])
+        response = SimpleNamespace(output=[item])
+        assert _get_output_text_from_response(response) == "world"
+
+    def test_empty_response(self):
+        response = SimpleNamespace()
+        assert _get_output_text_from_response(response) == ""
+
+
+class TestLLMCreateFallback:
+    @patch("openai_responses_agent.agent.OpenAI")
+    def _make_agent(self, mock_openai_cls):
+        mock_client = MagicMock()
+        mock_openai_cls.return_value = mock_client
+        agent = AIAgent(model="test-model", base_url="http://localhost:8000")
+        return agent, mock_client
+
+    def test_responses_api_success_caches_result(self):
+        agent, mock_client = self._make_agent()
+        mock_response = SimpleNamespace(
+            output=[
+                SimpleNamespace(
+                    content=[SimpleNamespace(type="output_text", text="ok")]
+                )
+            ]
+        )
+        mock_client.responses.create.return_value = mock_response
+
+        agent.messages = [{"role": "user", "content": "hi"}]
+        result = agent._llm_create(messages=agent.messages)
+
+        assert result is mock_response
+        assert agent._use_responses_api is True
+        mock_client.responses.create.assert_called_once()
+        mock_client.chat.completions.create.assert_not_called()
+
+    def test_fallback_on_400(self):
+        agent, mock_client = self._make_agent()
+        mock_response = MagicMock()
+        exc = APIStatusError(
+            message="Bad Request",
+            response=MagicMock(status_code=400, headers={}),
+            body=None,
+        )
+        mock_client.responses.create.side_effect = exc
+        mock_client.chat.completions.create.return_value = mock_response
+
+        agent.messages = [{"role": "user", "content": "hi"}]
+        result = agent._llm_create(messages=agent.messages)
+
+        assert result is mock_response
+        assert agent._use_responses_api is None
+        mock_client.chat.completions.create.assert_called_once()
+
+    def test_fallback_on_404(self):
+        agent, mock_client = self._make_agent()
+        mock_response = MagicMock()
+        exc = APIStatusError(
+            message="Not Found",
+            response=MagicMock(status_code=404, headers={}),
+            body=None,
+        )
+        mock_client.responses.create.side_effect = exc
+        mock_client.chat.completions.create.return_value = mock_response
+
+        agent.messages = [{"role": "user", "content": "hi"}]
+        result = agent._llm_create(messages=agent.messages)
+
+        assert result is mock_response
+        assert agent._use_responses_api is False
+
+    def test_non_fallback_error_propagates(self):
+        agent, mock_client = self._make_agent()
+        exc = APIStatusError(
+            message="Internal Server Error",
+            response=MagicMock(status_code=500, headers={}),
+            body=None,
+        )
+        mock_client.responses.create.side_effect = exc
+
+        agent.messages = [{"role": "user", "content": "hi"}]
+        with pytest.raises(APIStatusError):
+            agent._llm_create(messages=agent.messages)
+
+        assert agent._use_responses_api is None
+        mock_client.chat.completions.create.assert_not_called()
+
+    def test_cached_fallback_skips_probe(self):
+        agent, mock_client = self._make_agent()
+        mock_response = MagicMock()
+        mock_client.chat.completions.create.return_value = mock_response
+
+        agent._use_responses_api = False
+        agent.messages = [{"role": "user", "content": "hi"}]
+        result = agent._llm_create(messages=agent.messages)
+
+        assert result is mock_response
+        mock_client.responses.create.assert_not_called()
+        mock_client.chat.completions.create.assert_called_once()
+
+    def test_temperature_zero_is_passed(self):
+        """temperature=0 must be included in API kwargs, not omitted."""
+        agent, mock_client = self._make_agent()
+        mock_client.chat.completions.create.return_value = MagicMock()
+
+        agent._use_responses_api = False
+        agent.messages = [{"role": "user", "content": "hi"}]
+        agent._llm_create(messages=agent.messages)
+
+        call_kwargs = mock_client.chat.completions.create.call_args
+        assert call_kwargs[1]["temperature"] == 0
+
+    def test_fallback_on_400_after_prior_success(self):
+        """400 after a prior Responses API success falls back without caching."""
+        agent, mock_client = self._make_agent()
+        mock_response = MagicMock()
+        exc = APIStatusError(
+            message="Bad Request",
+            response=MagicMock(status_code=400, headers={}),
+            body=None,
+        )
+        mock_client.responses.create.side_effect = exc
+        mock_client.chat.completions.create.return_value = mock_response
+
+        agent._use_responses_api = True
+        agent.messages = [{"role": "user", "content": "multi-turn message"}]
+        result = agent._llm_create(messages=agent.messages)
+
+        assert result is mock_response
+        assert agent._use_responses_api is True
+        mock_client.chat.completions.create.assert_called_once()
+
+    def test_fallback_on_404_after_prior_success(self):
+        """404 after a prior Responses API success permanently disables it."""
+        agent, mock_client = self._make_agent()
+        mock_response = MagicMock()
+        exc = APIStatusError(
+            message="Not Found",
+            response=MagicMock(status_code=404, headers={}),
+            body=None,
+        )
+        mock_client.responses.create.side_effect = exc
+        mock_client.chat.completions.create.return_value = mock_response
+
+        agent._use_responses_api = True
+        agent.messages = [{"role": "user", "content": "multi-turn message"}]
+        result = agent._llm_create(messages=agent.messages)
+
+        assert result is mock_response
+        assert agent._use_responses_api is False
+        mock_client.chat.completions.create.assert_called_once()