diff --git a/litellm/model_prices_and_context_window_backup.json b/litellm/model_prices_and_context_window_backup.json
index e771cf12124..5d943e08503 100644
--- a/litellm/model_prices_and_context_window_backup.json
+++ b/litellm/model_prices_and_context_window_backup.json
@@ -5617,6 +5617,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
         "supports_prompt_caching": true,
         "supports_reasoning": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -5636,6 +5637,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
         "supports_prompt_caching": true,
         "supports_reasoning": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -11703,6 +11705,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -11741,6 +11744,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -11800,6 +11804,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -11819,6 +11824,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
         "supports_prompt_caching": true,
         "supports_reasoning": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -11932,6 +11938,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -11959,6 +11966,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12672,6 +12680,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12710,6 +12719,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12729,6 +12739,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
         "supports_prompt_caching": true,
         "supports_reasoning": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -12748,6 +12759,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
         "supports_prompt_caching": true,
         "supports_reasoning": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -12775,6 +12787,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12802,6 +12815,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -45620,6 +45634,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true,
         "supports_web_search": true
@@ -45741,6 +45756,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true,
         "supports_web_search": true
@@ -45764,6 +45780,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -45786,6 +45803,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -45912,6 +45930,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true,
         "supports_web_search": true
@@ -46013,6 +46032,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true,
         "supports_web_search": true
@@ -70127,6 +70147,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -71627,7 +71648,8 @@
             "search_context_size_low": 0.014,
             "search_context_size_medium": 0.014
         },
-        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'"
+        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
+        "supports_system_messages": true
     },
     "azure/eu/o3-2025-04-16": {
         "deprecation_date": "2026-11-19",
@@ -71646,7 +71668,8 @@
             "search_context_size_low": 0.014,
             "search_context_size_medium": 0.014
         },
-        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'"
+        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
+        "supports_system_messages": true
     },
     "azure/eu/o3-deep-research": {
         "deprecation_date": "2026-11-19",
@@ -71677,7 +71700,8 @@
             "search_context_size_low": 0.014,
             "search_context_size_medium": 0.014
         },
-        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'"
+        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
+        "supports_system_messages": true
     },
     "azure/eu/o4-mini-2025-04-16": {
         "deprecation_date": "2026-11-19",
@@ -71697,7 +71721,8 @@
             "search_context_size_low": 0.014,
             "search_context_size_medium": 0.014
         },
-        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'"
+        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
+        "supports_system_messages": true
     },
     "azure/eu/text-embedding-3-large": {
         "deprecation_date": "2028-02-09",
diff --git a/model_prices_and_context_window.json b/model_prices_and_context_window.json
index e771cf12124..5d943e08503 100644
--- a/model_prices_and_context_window.json
+++ b/model_prices_and_context_window.json
@@ -5617,6 +5617,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
         "supports_prompt_caching": true,
         "supports_reasoning": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -5636,6 +5637,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
         "supports_prompt_caching": true,
         "supports_reasoning": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -11703,6 +11705,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -11741,6 +11744,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -11800,6 +11804,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -11819,6 +11824,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
         "supports_prompt_caching": true,
         "supports_reasoning": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -11932,6 +11938,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -11959,6 +11966,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12672,6 +12680,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12710,6 +12719,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12729,6 +12739,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
         "supports_prompt_caching": true,
         "supports_reasoning": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -12748,6 +12759,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
         "supports_prompt_caching": true,
         "supports_reasoning": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -12775,6 +12787,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12802,6 +12815,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -45620,6 +45634,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true,
         "supports_web_search": true
@@ -45741,6 +45756,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true,
         "supports_web_search": true
@@ -45764,6 +45780,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -45786,6 +45803,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -45912,6 +45930,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true,
         "supports_web_search": true
@@ -46013,6 +46032,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true,
         "supports_web_search": true
@@ -70127,6 +70147,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -71627,7 +71648,8 @@
             "search_context_size_low": 0.014,
             "search_context_size_medium": 0.014
         },
-        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'"
+        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
+        "supports_system_messages": true
     },
     "azure/eu/o3-2025-04-16": {
         "deprecation_date": "2026-11-19",
@@ -71646,7 +71668,8 @@
             "search_context_size_low": 0.014,
             "search_context_size_medium": 0.014
         },
-        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'"
+        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
+        "supports_system_messages": true
     },
     "azure/eu/o3-deep-research": {
         "deprecation_date": "2026-11-19",
@@ -71677,7 +71700,8 @@
             "search_context_size_low": 0.014,
             "search_context_size_medium": 0.014
         },
-        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'"
+        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
+        "supports_system_messages": true
     },
     "azure/eu/o4-mini-2025-04-16": {
         "deprecation_date": "2026-11-19",
@@ -71697,7 +71721,8 @@
             "search_context_size_low": 0.014,
             "search_context_size_medium": 0.014
         },
-        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'"
+        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
+        "supports_system_messages": true
     },
     "azure/eu/text-embedding-3-large": {
         "deprecation_date": "2028-02-09",
diff --git a/tests/unit/llms/openai/test_o_series_transformation.py b/tests/unit/llms/openai/test_o_series_transformation.py
index 9d39dfda60a..a59928d83f2 100644
--- a/tests/unit/llms/openai/test_o_series_transformation.py
+++ b/tests/unit/llms/openai/test_o_series_transformation.py
@@ -6,6 +6,7 @@ import pytest
 
 import litellm
 from litellm import ModelResponse
+from litellm.llms.azure.chat.o_series_transformation import AzureOpenAIO1Config
 from litellm.llms.openai.chat.o_series_transformation import OpenAIOSeriesConfig
 import os
 
@@ -219,3 +220,24 @@ def test_o_series_request_turns_system_into_user_without_touching_the_callers_me
 
     assert [message["role"] for message in body["messages"]] == ["user", "user"]
     assert messages == messages_before
+
+
+@pytest.mark.parametrize(
+    "config",
+    [OpenAIOSeriesConfig(), AzureOpenAIO1Config()],
+    ids=["openai", "azure"],
+)
+@pytest.mark.parametrize("model", ["o3", "o3-2025-04-16", "o4-mini", "o4-mini-2025-04-16", "o3-mini"])
+def test_o_series_keeps_system_role_for_models_that_support_it(config: OpenAIOSeriesConfig, model: str):
+    """o1-2024-12-17 and later reasoning models accept system messages, which the API treats as developer messages
+    (https://platform.openai.com/docs/guides/reasoning, checked 2026-10-28). Rewriting them as user messages drops
+    them to user-level authority"""
+    system_message: Final = {"role": "system", "content": "Be a good bot!"}
+    request: Final = config.transform_request(
+        model=model,
+        messages=[dict(system_message), {"role": "user", "content": "hi"}],
+        optional_params={},
+        litellm_params={},
+        headers={},
+    )
+    assert request["messages"][0] == system_message