diff --git a/litellm/proxy/proxy_server.py b/litellm/proxy/proxy_server.py
index 76ef3e3b541..450b66745d4 100644
--- a/litellm/proxy/proxy_server.py
+++ b/litellm/proxy/proxy_server.py
@@ -350,6 +350,7 @@ from litellm.constants import (
     WEEKLY_SPEND_REPORT_JOB_ID,
 )
 from litellm.exceptions import RejectedRequestError
+from litellm.google_genai.adapters.transformation import GoogleGenAIAdapter
 from litellm.integrations.custom_guardrail import CustomGuardrail, ModifyResponseException
 from litellm.integrations.custom_logger import CustomLogger
 from litellm.integrations.SlackAlerting.slack_alerting import SlackAlerting
@@ -14762,6 +14763,24 @@ def _counted_request_messages(
     return list(drop_non_string_tool_result_texts(messages, deployment_drops_params(deployment)))
 
 
+_LOCALLY_COUNTED_MESSAGES: Final = TypeAdapter(list[dict[str, object]])
+
+
+def _locally_counted_messages(
+    request_messages: list[dict[str, object]] | None,  # mutable-ok: _counted_request_messages returns list messages
+    contents: Sequence[Mapping[str, object]] | None,
+    model: str,
+) -> list[dict[str, object]] | None:  # mutable-ok: token_counter takes list messages
+    if request_messages or not contents:
+        return request_messages
+    translate: Final = cast(  # cast-ok: the adapter's untyped **kwargs leave its signature partially unknown
+        Callable[[str, list[dict[str, object]]], Mapping[str, object]],
+        GoogleGenAIAdapter().translate_generate_content_to_completion,
+    )
+    translated: Final = translate(model, [dict(content) for content in contents])
+    return _LOCALLY_COUNTED_MESSAGES.validate_python(translated.get("messages", []))
+
+
 async def _try_provider_token_count(
     provider_counter: "BaseTokenCounter",
     custom_llm_provider: str | None,
@@ -15413,7 +15432,19 @@ async def count_request_tokens(
     prompt_turn: Final = prompt_only and not (system_message is None and not tools)
     typed_messages: Final = cast(  # cast-ok: request messages are raw chat-shaped dicts that token_counter normalizes
         Sequence[AllMessageValues] | None,
-        [{"role": "user", "content": prompt}] if prompt_turn else (None if prompt_only else request_messages),
+        [{"role": "user", "content": prompt}]
+        if prompt_turn
+        else (
+            None
+            if prompt_only
+            else _locally_counted_messages(
+                request_messages,
+                cast(  # cast-ok: TokenCountRequest.contents is typed list[dict], the local counter needs str-keyed parts
+                    Sequence[Mapping[str, object]] | None, contents
+                ),
+                model_to_use,
+            )
+        ),
     )
     counted_messages: Final = (
         typed_messages if typed_messages is None or system_message is None else (system_message, *typed_messages)
diff --git a/tests/integration/providers/test_vertex_gemini_count_tokens_wire.py b/tests/integration/providers/test_vertex_gemini_count_tokens_wire.py
index 5c08fddd4b8..214bee77895 100644
--- a/tests/integration/providers/test_vertex_gemini_count_tokens_wire.py
+++ b/tests/integration/providers/test_vertex_gemini_count_tokens_wire.py
@@ -1043,8 +1043,13 @@ def test_utils_token_counter_sends_a_prompt_as_the_user_turn_of_its_messages_for
 
 @pytest.mark.parametrize(
     ("conversation", "call_endpoint"),
-    (({"messages": _MESSAGES}, True), ({"contents": _CONTENTS}, True), ({"messages": _MESSAGES}, False)),
-    ids=("provider-count-messages", "provider-count-contents", "local-count-messages"),
+    (
+        ({"messages": _MESSAGES}, True),
+        ({"contents": _CONTENTS}, True),
+        ({"messages": _MESSAGES}, False),
+        ({"contents": _CONTENTS}, False),
+    ),
+    ids=("provider-count-messages", "provider-count-contents", "local-count-messages", "local-count-contents"),
 )
 @pytest.mark.parametrize("drop_params", (False, True), ids=("no-drop", "drop"))
 def test_utils_token_counter_counts_the_conversation_regardless_of_prompt_and_drop_params(
diff --git a/tests/unit/proxy/test_proxy_token_counter.py b/tests/unit/proxy/test_proxy_token_counter.py
index 436694c3849..be7e50adf62 100644
--- a/tests/unit/proxy/test_proxy_token_counter.py
+++ b/tests/unit/proxy/test_proxy_token_counter.py
@@ -3422,8 +3422,13 @@ _CONVERSATIONS: Final = (
 @pytest.mark.asyncio
 @pytest.mark.parametrize(
     ("conversation", "call_endpoint"),
-    ((_CONVERSATIONS[0], True), (_CONVERSATIONS[1], True), (_CONVERSATIONS[0], False)),
-    ids=("provider_messages", "provider_contents", "local_messages"),
+    (
+        (_CONVERSATIONS[0], True),
+        (_CONVERSATIONS[1], True),
+        (_CONVERSATIONS[0], False),
+        (_CONVERSATIONS[1], False),
+    ),
+    ids=("provider_messages", "provider_contents", "local_messages", "local_contents"),
 )
 @pytest.mark.parametrize(
     ("global_drop_params", "deployment_drop_params"),