diff --git a/src/transformers/commands/serving.py b/src/transformers/commands/serving.py
index 06a3bc6b92..d8d7d1b22b 100644
--- a/src/transformers/commands/serving.py
+++ b/src/transformers/commands/serving.py
@@ -396,6 +396,9 @@ class ServeArguments:
     log_level: str = field(
         default="info", metadata={"help": "Logging level as a string. Example: 'info' or 'warning'."}
     )
+    default_seed: Optional[int] = field(
+        default=None, metadata={"help": "The default seed for torch, should be an integer."}
+    )
     enable_cors: bool = field(
         default=False,
         metadata={
@@ -451,6 +454,9 @@ class ServeCommand(BaseTransformersCLICommand):
         self.use_continuous_batching = self.args.attn_implementation == "sdpa_paged"
         self.enable_cors = self.args.enable_cors
 
+        if self.args.default_seed is not None:
+            torch.manual_seed(self.args.default_seed)
+
         # Set up logging
         transformers_logger = logging.get_logger("transformers")
         transformers_logger.setLevel(logging.log_levels[self.args.log_level.lower()])
@@ -1032,7 +1038,26 @@ class ServeCommand(BaseTransformersCLICommand):
         self.last_model = model_id_and_revision
         model, processor = self.load_model_and_processor(model_id_and_revision)
 
-        inputs = processor.apply_chat_template(req["input"], add_generation_prompt=True).to(model.device)
+        if isinstance(req["input"], str):
+            inputs = [{"role": "system", "content": req["instructions"]}] if "instructions" in req else []
+            inputs.append({"role": "user", "content": req["input"]})
+        elif isinstance(req["input"], list):
+            if "instructions" in req:
+                if req["input"][0]["role"] != "system":
+                    inputs = [{"role": "system", "content": req["instructions"]}, *req["input"]]
+                else:
+                    inputs = req["input"]
+                    inputs[0]["content"] = req["instructions"]
+            else:
+                inputs = req["input"]
+        elif isinstance(req["input"], dict):
+            inputs = [{"role": "system", "content": req["instructions"]}] if "instructions" in req else []
+            inputs.append(req["input"])
+        else:
+            raise ValueError("inputs should be a list, dict, or str")
+
+        inputs = processor.apply_chat_template(inputs, add_generation_prompt=True, return_tensors="pt")
+        inputs = inputs.to(model.device)
         request_id = req.get("previous_response_id", "req_0")
 
         generation_streamer = TextIteratorStreamer(processor, skip_special_tokens=True, skip_prompt=True)
diff --git a/tests/commands/test_serving.py b/tests/commands/test_serving.py
index f0592686e8..87b5f61e2c 100644
--- a/tests/commands/test_serving.py
+++ b/tests/commands/test_serving.py
@@ -30,8 +30,20 @@ from transformers.utils.import_utils import is_openai_available
 
 
 if is_openai_available():
+    from openai import APIConnectionError, OpenAI
     from openai.types.chat.chat_completion_chunk import ChoiceDeltaToolCall, ChoiceDeltaToolCallFunction
-    from openai.types.responses import Response, ResponseCreatedEvent
+    from openai.types.responses import (
+        Response,
+        ResponseCompletedEvent,
+        ResponseContentPartAddedEvent,
+        ResponseContentPartDoneEvent,
+        ResponseCreatedEvent,
+        ResponseInProgressEvent,
+        ResponseOutputItemAddedEvent,
+        ResponseOutputItemDoneEvent,
+        ResponseTextDeltaEvent,
+        ResponseTextDoneEvent,
+    )
 
 
 @require_openai
@@ -156,7 +168,7 @@ def async_retry(fn, max_attempts=5, delay=2):
         for _ in range(max_attempts):
             try:
                 return await fn(*args, **kwargs)
-            except aiohttp.client_exceptions.ClientConnectorError:
+            except (aiohttp.client_exceptions.ClientConnectorError, APIConnectionError):
                 time.sleep(delay)
 
     return wrapper
@@ -465,4 +477,94 @@ class ServeCompletionsContinuousBatchingIntegrationTest(ServeCompletionsMixin, u
         thread.start()
 
 
-# TODO: Response integration tests
+@require_openai
+class ServeResponsesMixin:
+    """
+    Mixin class for the Completions API tests, to seamlessly replicate tests across the two versions of the API
+    (`generate` and `continuous_batching`).
+    """
+
+    @async_retry
+    async def run_server(self, request):
+        client = OpenAI(base_url=f"http://localhost:{self.port}/v1", api_key="<KEY>")
+        stream = client.responses.create(**request)
+
+        all_payloads = []
+        for payload in stream:
+            all_payloads.append(payload)
+
+        return all_payloads
+
+    def test_request(self):
+        """Tests that an inference using the Responses API works"""
+
+        request = {
+            "model": "Qwen/Qwen2.5-0.5B-Instruct",
+            "instructions": "You are a helpful assistant.",
+            "input": "Hello!",
+            "stream": True,
+            "max_output_tokens": 1,
+        }
+        all_payloads = asyncio.run(self.run_server(request))
+        print("ok")
+
+        order_of_payloads = [
+            ResponseCreatedEvent,
+            ResponseInProgressEvent,
+            ResponseOutputItemAddedEvent,
+            ResponseContentPartAddedEvent,
+            ResponseTextDeltaEvent,
+            ResponseTextDeltaEvent,
+            ResponseTextDoneEvent,
+            ResponseContentPartDoneEvent,
+            ResponseOutputItemDoneEvent,
+            ResponseCompletedEvent,
+        ]
+
+        self.assertEqual(len(all_payloads), 10)
+        for payload, payload_type in zip(all_payloads, order_of_payloads):
+            self.assertIsInstance(payload, payload_type)
+
+    # TODO: one test for each request flag, to confirm it is working as expected
+    # TODO: speed-based test to confirm that KV cache is working across requests
+
+
+@slow  # server startup time is slow on our push CI
+@require_openai
+class ServeResponsesIntegrationTest(ServeResponsesMixin, unittest.TestCase):
+    """Tests the Responses API."""
+
+    @classmethod
+    def setUpClass(cls):
+        """Starts a server for tests to connect to."""
+        cls.port = 8003
+        args = ServeArguments(port=cls.port, default_seed=42)
+        serve_command = ServeCommand(args)
+        thread = Thread(target=serve_command.run)
+        thread.daemon = True
+        thread.start()
+
+    @slow
+    def test_full_request(self):
+        """Tests that an inference using the Responses API works"""
+
+        request = {
+            "model": "Qwen/Qwen2.5-0.5B-Instruct",
+            "instructions": "You are a sports assistant designed to craft sports programs.",
+            "input": "Tell me what you can do.",
+            "stream": True,
+            "max_output_tokens": 30,
+        }
+        all_payloads = asyncio.run(self.run_server(request))
+
+        full_text = ""
+        for token in all_payloads:
+            if isinstance(token, ResponseTextDeltaEvent):
+                full_text += token.delta
+
+        # Verify that the system prompt went through.
+        self.assertTrue(
+            full_text.startswith(
+                "As an AI language model, I am designed to assist with various tasks and provide information on different topics related to sports."
+            )
+        )