diff --git a/litellm/responses/litellm_completion_transformation/transformation.py b/litellm/responses/litellm_completion_transformation/transformation.py
index cc594f167c7..1738cfc5da7 100644
--- a/litellm/responses/litellm_completion_transformation/transformation.py
+++ b/litellm/responses/litellm_completion_transformation/transformation.py
@@ -434,22 +434,59 @@ class LiteLLMCompletionResponsesConfig:
             | ChatCompletionResponseMessage
             | Message
         ] = []
-        if responses_api_request.get("instructions"):
-            messages.append(
-                LiteLLMCompletionResponsesConfig.transform_instructions_to_system_message(
-                    responses_api_request.get("instructions")
-                )
-            )
-
-        messages.extend(
+        input_messages: Final = tuple(
             LiteLLMCompletionResponsesConfig._transform_response_input_param_to_chat_completion_message(
                 input=input,
                 replay_reasoning=replay_reasoning,
             )
         )
 
+        # `instructions` and the input can each carry a system message, which left a
+        # conversation reading system, user, system. Chat templates that require the
+        # system message first reject that, so gather them into one leading message.
+        instructions: Final = responses_api_request.get("instructions")
+        system_contents: Final = tuple(
+            content
+            for content in (
+                instructions,
+                *(message.get("content") for message in input_messages if message.get("role") == "system"),
+            )
+            if content
+        )
+
+        if system_contents:
+            messages.append(LiteLLMCompletionResponsesConfig._merge_system_contents(system_contents))
+
+        messages.extend(message for message in input_messages if message.get("role") != "system")
+
         return messages
 
+    @staticmethod
+    def _merge_system_contents(contents: tuple[Any, ...]) -> ChatCompletionSystemMessage:
+        """Join system prompts into one leading message.
+
+        Part lists collapse to their text: system content is conventionally a string, and
+        the backends that reject a trailing system message are the same ones that expect one.
+        """
+        texts: Final = tuple(
+            text for content in contents for text in LiteLLMCompletionResponsesConfig._system_content_texts(content)
+        )
+        return ChatCompletionSystemMessage(role="system", content="\n\n".join(text for text in texts if text))
+
+    @staticmethod
+    def _system_content_texts(content: object) -> tuple[str, ...]:
+        """Every text a system content field carries, as a plain string or as a part list
+        that may mix bare strings with text parts."""
+        if isinstance(content, str):
+            return (content,)
+        if not isinstance(content, (list, tuple)):
+            return ()
+        return tuple(
+            part if isinstance(part, str) else str(part.get("text", ""))
+            for part in content
+            if isinstance(part, (str, dict))
+        )
+
     @staticmethod
     async def async_responses_api_session_handler(
         previous_response_id: str,
diff --git a/tests/test_litellm/responses/litellm_completion_transformation/test_system_message_hoisting.py b/tests/test_litellm/responses/litellm_completion_transformation/test_system_message_hoisting.py
new file mode 100644
index 00000000000..4b91694d73b
--- /dev/null
+++ b/tests/test_litellm/responses/litellm_completion_transformation/test_system_message_hoisting.py
@@ -0,0 +1,89 @@
+"""
+Unit tests for keeping system messages at the front of the bridged chat request.
+
+``instructions`` becomes a leading system message and the Responses input can carry
+a system message of its own, so an Anthropic ``/v1/messages`` conversation bridged
+to chat completions could come out as system, user, system. Chat templates that
+require the system message to come first reject that with
+"System message must be at the beginning".
+
+See: https://github.com/BerriAI/litellm/issues/40693
+"""
+
+from litellm.responses.litellm_completion_transformation.transformation import (
+    LiteLLMCompletionResponsesConfig,
+)
+
+
+def _roles(input, responses_api_request):
+    messages = LiteLLMCompletionResponsesConfig.transform_responses_api_input_to_messages(
+        input=input, responses_api_request=responses_api_request
+    )
+    return [message.get("role") for message in messages], messages
+
+
+def test_system_message_after_user_content_is_hoisted():
+    roles, messages = _roles(
+        [
+            {"role": "user", "content": "first question"},
+            {"role": "system", "content": "mid"},
+            {"role": "user", "content": "second question"},
+        ],
+        {"instructions": "lead"},
+    )
+
+    assert roles == ["system", "user", "user"]
+    assert "system" not in roles[1:]
+
+
+def test_both_system_prompts_survive_the_merge():
+    _, messages = _roles(
+        [
+            {"role": "user", "content": "q"},
+            {"role": "system", "content": "mid"},
+        ],
+        {"instructions": "lead"},
+    )
+
+    assert messages[0]["content"] == "lead\n\nmid"
+
+
+def test_part_list_content_collapses_to_its_text():
+    """A system message given as parts still contributes its text to the merged prompt."""
+    _, messages = _roles(
+        [
+            {"role": "user", "content": "q"},
+            {"role": "system", "content": [{"type": "text", "text": "B"}]},
+        ],
+        {"instructions": "A"},
+    )
+
+    assert messages[0]["content"] == "A\n\nB"
+
+
+def test_an_already_leading_system_message_is_left_alone():
+    """The common case must not be rewritten."""
+    roles, messages = _roles([{"role": "user", "content": "q"}], {"instructions": "lead"})
+
+    assert roles == ["system", "user"]
+    assert messages[0]["content"] == "lead"
+
+
+def test_a_conversation_without_a_system_message_is_unchanged():
+    roles, _ = _roles([{"role": "user", "content": "q"}], {})
+
+    assert roles == ["user"]
+
+
+def test_bare_strings_in_a_part_list_survive_the_merge():
+    """Upstream normalization leaves plain strings in a content list, so filtering the
+    list down to dicts silently dropped part of the prompt."""
+    _, messages = _roles(
+        [
+            {"role": "user", "content": "q"},
+            {"role": "system", "content": ["B", {"type": "text", "text": "C"}]},
+        ],
+        {"instructions": "A"},
+    )
+
+    assert messages[0]["content"] == "A\n\nB\n\nC"