diff --git a/litellm/completion_extras/litellm_responses_transformation/transformation.py b/litellm/completion_extras/litellm_responses_transformation/transformation.py
index c25d7bd9410..d6c73aef03c 100644
--- a/litellm/completion_extras/litellm_responses_transformation/transformation.py
+++ b/litellm/completion_extras/litellm_responses_transformation/transformation.py
@@ -129,6 +129,35 @@ def _breakpoint_of(part: object) -> object:
     return content_part.get("prompt_cache_breakpoint")
 
 
+def _foldable_system_text(block: object) -> str | None:
+    if isinstance(block, str):
+        return block
+    if not isinstance(block, dict):
+        return None
+    text_block: Final = cast(dict[str, object], block)  # cast-ok: isinstance confirms a content block mapping
+    text: Final = text_block.get("text")
+    if text_block.get("type") != "text" or not isinstance(text, str) or _breakpoint_of(text_block) is not None:
+        return None
+    return text
+
+
+def _system_text_for_instructions(message: Mapping[str, object]) -> str | None:
+    """A leading system message's text for ``instructions``, or None to keep it a positioned input item.
+
+    List content folds when every block is plain text, the shape a client attaching cache_control sends.
+    A non-text block (an image, say) would be lost in a string, and a prompt_cache_breakpoint only rides
+    on an input item's content block, so either keeps the message an input item.
+    """
+    content: Final = message.get("content", "")
+    if isinstance(content, str):
+        return content
+    if not isinstance(content, list):
+        return None
+    blocks: Final = cast(list[object], content)  # cast-ok: isinstance confirms a list of content blocks
+    texts: Final = tuple(text for text in map(_foldable_system_text, blocks) if text is not None)
+    return " ".join(texts) if len(texts) == len(blocks) else None
+
+
 def _pending_audio_breakpoint(pending: object, part: object) -> object:
     if not _is_audio_input_part(part):
         return None
@@ -536,24 +565,9 @@ class LiteLLMResponsesTransformationHandler(CompletionTransformationBridge):
             tool_call_id = msg.get("tool_call_id")
 
             if role == "system":
-                # Extract system message as instructions, but only within the leading run of
-                # system messages: a later one stays a positioned input item so its bytes don't
-                # unsettle the prompt-cache-stable prefix (#40269).
-                extracted_instructions: str | None = None
-                if index < leading_system_count:
-                    if isinstance(content, str):
-                        extracted_instructions = content
-                    elif isinstance(content, list) and all(
-                        isinstance(block, str) or (isinstance(block, dict) and block.get("type") == "text")
-                        for block in content
-                    ):
-                        # Every block is plain text (a bare string or a `{"type": "text", ...}`
-                        # dict), the same shape a client attaching cache_control sends; a
-                        # non-text block (an image, say) fails the `all()` above and falls
-                        # through to the input-item branch below instead of losing it silently.
-                        extracted_instructions = " ".join(
-                            block if isinstance(block, str) else block.get("text", "") for block in content
-                        )
+                # Only the leading run of system messages folds into instructions: a later one stays
+                # a positioned input item so its bytes don't unsettle the cached prefix (#40269).
+                extracted_instructions = _system_text_for_instructions(msg) if index < leading_system_count else None
                 if extracted_instructions is not None:
                     if instructions:
                         # Concatenate multiple system prompts with a space
diff --git a/tests/unit/completion_extras/litellm_responses_transformation/test_completion_extras_litellm_responses_transformation_transformation.py b/tests/unit/completion_extras/litellm_responses_transformation/test_completion_extras_litellm_responses_transformation_transformation.py
index 82a23a0f8be..10527607308 100644
--- a/tests/unit/completion_extras/litellm_responses_transformation/test_completion_extras_litellm_responses_transformation_transformation.py
+++ b/tests/unit/completion_extras/litellm_responses_transformation/test_completion_extras_litellm_responses_transformation_transformation.py
@@ -4887,6 +4887,26 @@ def test_leading_system_list_with_a_non_text_block_stays_an_input_item():
     assert input_items[0]["content"][1]["type"] == "input_image"
 
 
+def test_leading_system_list_with_a_prompt_cache_breakpoint_stays_an_input_item():
+    """A prompt_cache_breakpoint rides only on an input item's content block, so a leading
+    system message carrying one stays an input item and keeps its marker rather than folding."""
+    handler: Final = LiteLLMResponsesTransformationHandler()
+
+    input_items, instructions = handler.convert_chat_completion_messages_to_responses_api(
+        [
+            {"role": "system", "content": [_MARKED_SYSTEM_PART]},
+            {"role": "user", "content": "hi"},
+        ],
+        keep_prompt_cache_breakpoints=True,
+    )
+
+    assert instructions is None
+    assert input_items == [
+        {"type": "message", "role": "system", "content": [{**_MARKED_SYSTEM_PART, "type": "input_text"}]},
+        {"type": "message", "role": "user", "content": [{"type": "input_text", "text": "hi"}]},
+    ]
+
+
 def test_map_optional_params_verbosity_merges_into_text():
     """Chat verbosity must land on Responses text.verbosity alongside text.format regardless of key order."""
     from litellm.completion_extras.litellm_responses_transformation.transformation import (