diff --git a/litellm/llms/openai/responses/count_tokens/transformation.py b/litellm/llms/openai/responses/count_tokens/transformation.py
index 72038ae6f6c..62dbebb4fe6 100644
--- a/litellm/llms/openai/responses/count_tokens/transformation.py
+++ b/litellm/llms/openai/responses/count_tokens/transformation.py
@@ -23,6 +23,8 @@ class ResponsesInputImagePart(TypedDict):
 
 ResponsesInputPart = ResponsesInputTextPart | ResponsesInputImagePart
 
+ResponsesContentRole = Literal["user", "assistant"]
+
 
 def _chat_image_block_to_responses_part(image_url: object) -> ResponsesInputImagePart | None:
     url: Final = image_url.get("url") if isinstance(image_url, Mapping) else image_url
@@ -37,7 +39,7 @@ def _chat_image_block_to_responses_part(image_url: object) -> ResponsesInputImag
     return part
 
 
-def _chat_block_to_responses_part(block: object) -> ResponsesInputPart | None:
+def _chat_block_to_responses_part(block: object, role: ResponsesContentRole) -> ResponsesInputPart | None:
     if isinstance(block, str):
         bare: Final[ResponsesInputTextPart] = {"type": "input_text", "text": block}
         return bare
@@ -51,7 +53,7 @@ def _chat_block_to_responses_part(block: object) -> ResponsesInputPart | None:
                 "text": text_value if isinstance(text_value, str) else "",
             }
             return text
-        case "image_url":
+        case "image_url" if role == "user":
             return _chat_image_block_to_responses_part(block.get("image_url"))
         case _:
             return None
@@ -59,10 +61,15 @@ def _chat_block_to_responses_part(block: object) -> ResponsesInputPart | None:
 
 def chat_content_blocks_to_responses_content(
     content: Sequence[object],
+    role: ResponsesContentRole,
 ) -> str | tuple[ResponsesInputPart, ...]:
-    """Text-only content collapses to a joined string, so text-only counts stay unchanged."""
+    """Text-only content collapses to a joined string, which every role accepts and counts identically.
+
+    Only a user turn may carry an image part: the Responses API rejects any part but
+    output_text and refusal inside an assistant turn.
+    """
     parts: Final = tuple(
-        part for part in (_chat_block_to_responses_part(block) for block in content) if part is not None
+        part for part in (_chat_block_to_responses_part(block, role) for block in content) if part is not None
     )
     if any(part["type"] != "input_text" for part in parts):
         return parts
@@ -182,11 +189,13 @@ class OpenAICountTokensConfig:
                     instructions_parts.append("\n".join(text_parts))
             elif role == "user":
                 if isinstance(content, list):
-                    content = chat_content_blocks_to_responses_content(content)
+                    content = chat_content_blocks_to_responses_content(content, "user")
                 input_items.append({"role": "user", "content": content})
             elif role == "assistant":
                 # Map tool_calls to Responses API function_call items
                 tool_calls = msg.get("tool_calls")
+                if isinstance(content, list):
+                    content = chat_content_blocks_to_responses_content(content, "assistant")
                 if content:
                     input_items.append({"role": "assistant", "content": content})
                 if tool_calls:
diff --git a/tests/test_litellm/llms/openai/responses/test_openai_count_tokens_transformation.py b/tests/test_litellm/llms/openai/responses/test_openai_count_tokens_transformation.py
index ca9e7ab52c3..22761272321 100644
--- a/tests/test_litellm/llms/openai/responses/test_openai_count_tokens_transformation.py
+++ b/tests/test_litellm/llms/openai/responses/test_openai_count_tokens_transformation.py
@@ -260,6 +260,69 @@ def test_messages_to_responses_input_drops_unmappable_blocks():
     )
 
 
+def test_messages_to_responses_input_assistant_blocks_collapse_to_a_string():
+    """An assistant turn must never forward chat `text` blocks.
+
+    The Responses API only accepts output_text and refusal inside an assistant turn, so
+    forwarding them 400s the whole request and silently drops the count back to the local
+    tokenizer, which is exactly what defeats the image fix above.
+    """
+    messages = [
+        {"role": "user", "content": [{"type": "text", "text": "What is the capital of France?"}]},
+        {"role": "assistant", "content": [{"type": "text", "text": "Paris."}]},
+    ]
+
+    input_items, _ = OpenAICountTokensConfig.messages_to_responses_input(messages)
+
+    assert input_items == [
+        {"role": "user", "content": "What is the capital of France?"},
+        {"role": "assistant", "content": "Paris."},
+    ]
+
+
+def test_messages_to_responses_input_assistant_image_block_is_dropped():
+    """An image part is illegal inside an assistant turn, so it must not reach the provider."""
+    messages = [
+        {
+            "role": "assistant",
+            "content": [
+                {"type": "text", "text": "Here it is"},
+                {"type": "image_url", "image_url": {"url": "https://example.com/cat.png"}},
+            ],
+        }
+    ]
+
+    input_items, _ = OpenAICountTokensConfig.messages_to_responses_input(messages)
+
+    assert input_items == [{"role": "assistant", "content": "Here it is"}]
+
+
+def test_messages_to_responses_input_keeps_user_image_alongside_an_assistant_turn():
+    messages = [
+        {
+            "role": "user",
+            "content": [
+                {"type": "text", "text": "What is in this image?"},
+                {"type": "image_url", "image_url": {"url": "https://example.com/cat.png"}},
+            ],
+        },
+        {"role": "assistant", "content": [{"type": "text", "text": "A cat."}]},
+    ]
+
+    input_items, _ = OpenAICountTokensConfig.messages_to_responses_input(messages)
+
+    assert input_items == [
+        {
+            "role": "user",
+            "content": (
+                {"type": "input_text", "text": "What is in this image?"},
+                {"type": "input_image", "image_url": "https://example.com/cat.png", "detail": "auto"},
+            ),
+        },
+        {"role": "assistant", "content": "A cat."},
+    ]
+
+
 def test_validate_request_valid():
     """Test that valid requests pass validation."""
     config = OpenAICountTokensConfig()