diff --git a/litellm/responses/litellm_completion_transformation/transformation.py b/litellm/responses/litellm_completion_transformation/transformation.py
index 48b12a5fba9..ce4293e9743 100644
--- a/litellm/responses/litellm_completion_transformation/transformation.py
+++ b/litellm/responses/litellm_completion_transformation/transformation.py
@@ -282,7 +282,81 @@ class LiteLLMCompletionResponsesConfig:
             )
         )
 
-        return messages
+        return LiteLLMCompletionResponsesConfig._merge_responses_system_messages(
+            messages=messages
+        )
+
+    @staticmethod
+    def _get_text_from_message_content(content: Any) -> str:
+        if content is None:
+            return ""
+        if isinstance(content, str):
+            return content
+        if isinstance(content, list):
+            text_parts: List[str] = []
+            for content_part in content:
+                if isinstance(content_part, str):
+                    text_parts.append(content_part)
+                elif isinstance(content_part, dict):
+                    content_type = content_part.get("type")
+                    text = content_part.get("text")
+                    if content_type in {"text", "input_text"} and isinstance(text, str):
+                        text_parts.append(text)
+            return "\n\n".join(text_parts)
+        return str(content)
+
+    @staticmethod
+    def _merge_responses_system_messages(
+        messages: List[
+            Union[
+                AllMessageValues,
+                GenericChatCompletionMessage,
+                ChatCompletionMessageToolCall,
+                ChatCompletionResponseMessage,
+                Message,
+            ]
+        ],
+    ) -> List[
+        Union[
+            AllMessageValues,
+            GenericChatCompletionMessage,
+            ChatCompletionMessageToolCall,
+            ChatCompletionResponseMessage,
+            Message,
+        ]
+    ]:
+        system_parts: List[str] = []
+        non_system_messages: List[
+            Union[
+                AllMessageValues,
+                GenericChatCompletionMessage,
+                ChatCompletionMessageToolCall,
+                ChatCompletionResponseMessage,
+                Message,
+            ]
+        ] = []
+
+        for message in messages:
+            role = message.get("role") if isinstance(message, dict) else None
+            if role in {"system", "developer"}:
+                content = message.get("content") if isinstance(message, dict) else None
+                text_content = (
+                    LiteLLMCompletionResponsesConfig._get_text_from_message_content(
+                        content=content
+                    )
+                )
+                if text_content:
+                    system_parts.append(text_content)
+                continue
+            non_system_messages.append(message)
+
+        if not system_parts:
+            return messages
+
+        system_message = ChatCompletionSystemMessage(
+            role="system", content="\n\n".join(system_parts)
+        )
+        return [system_message, *non_system_messages]
 
     @staticmethod
     async def async_responses_api_session_handler(
diff --git a/tests/test_litellm/responses/litellm_completion_transformation/test_litellm_completion_responses.py b/tests/test_litellm/responses/litellm_completion_transformation/test_litellm_completion_responses.py
index 5d8ff8022e5..fdd96d26050 100644
--- a/tests/test_litellm/responses/litellm_completion_transformation/test_litellm_completion_responses.py
+++ b/tests/test_litellm/responses/litellm_completion_transformation/test_litellm_completion_responses.py
@@ -808,6 +808,98 @@ class TestFunctionCallTransformation:
 
         assert result["extra_headers"] == {"X-Test-Header": "test-value"}
 
+    def test_request_transformation_merges_instructions_and_developer_messages(self):
+        """Responses instructions and developer messages should become one system message."""
+        test_input = [
+            {
+                "type": "message",
+                "role": "developer",
+                "content": "Use concise responses.",
+            },
+            {
+                "type": "message",
+                "role": "developer",
+                "content": [{"type": "input_text", "text": "Never expose secrets."}],
+            },
+            {
+                "type": "message",
+                "role": "user",
+                "content": "Hello",
+            },
+        ]
+        responses_api_request = {"instructions": "You are helpful."}
+
+        result = LiteLLMCompletionResponsesConfig.transform_responses_api_request_to_chat_completion_request(
+            model="custom_openai/qwen",
+            input=test_input,
+            responses_api_request=responses_api_request,
+        )
+
+        messages = result["messages"]
+        assert messages == [
+            {
+                "role": "system",
+                "content": "You are helpful.\n\nUse concise responses.\n\nNever expose secrets.",
+            },
+            {"role": "user", "content": "Hello"},
+        ]
+
+    def test_request_transformation_preserves_messages_without_system_content(self):
+        """Requests without instructions/developer content should not be rewritten."""
+        test_input = [
+            {
+                "type": "message",
+                "role": "user",
+                "content": "Hello",
+            },
+            {
+                "type": "message",
+                "role": "assistant",
+                "content": "Hi there",
+            },
+        ]
+
+        result = LiteLLMCompletionResponsesConfig.transform_responses_api_request_to_chat_completion_request(
+            model="custom_openai/qwen",
+            input=test_input,
+            responses_api_request={},
+        )
+
+        assert result["messages"] == [
+            {"role": "user", "content": "Hello"},
+            {"role": "assistant", "content": "Hi there"},
+        ]
+
+    def test_merge_responses_system_messages_extracts_supported_text_content(self):
+        """System/developer content blocks should merge only supported text parts."""
+        messages = [
+            {"role": "system", "content": None},
+            {
+                "role": "developer",
+                "content": [
+                    "Plain text",
+                    {"type": "text", "text": "Text block"},
+                    {"type": "input_text", "text": "Input text block"},
+                    {"type": "image_url", "text": "Ignored image text"},
+                    {"type": "text", "text": 123},
+                ],
+            },
+            {"role": "developer", "content": 123},
+            {"role": "user", "content": "Hello"},
+        ]
+
+        result = LiteLLMCompletionResponsesConfig._merge_responses_system_messages(
+            messages=messages
+        )
+
+        assert result == [
+            {
+                "role": "system",
+                "content": "Plain text\n\nText block\n\nInput text block\n\n123",
+            },
+            {"role": "user", "content": "Hello"},
+        ]
+
     def test_function_call_without_call_id_fallback_to_id(self):
         """Test that function_call items can use 'id' field when 'call_id' is missing"""
         function_call_item = {