diff --git a/litellm/model_prices_and_context_window_backup.json b/litellm/model_prices_and_context_window_backup.json
index c6bbb63b6fc..5fb0ab11873 100644
--- a/litellm/model_prices_and_context_window_backup.json
+++ b/litellm/model_prices_and_context_window_backup.json
@@ -5359,6 +5359,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
         "supports_prompt_caching": true,
         "supports_reasoning": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -5376,6 +5377,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$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
     },
@@ -11330,6 +11332,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -11367,6 +11370,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -11419,6 +11423,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -11436,6 +11441,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
         "supports_prompt_caching": true,
         "supports_reasoning": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -11540,6 +11546,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -11565,6 +11572,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12267,6 +12275,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12304,6 +12313,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12321,6 +12331,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$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
     },
@@ -12338,6 +12349,7 @@
         "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
     },
@@ -12363,6 +12375,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12388,6 +12401,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -44525,6 +44539,7 @@
         "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
@@ -44640,6 +44655,7 @@
         "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
@@ -44661,6 +44677,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -44681,6 +44698,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -44801,6 +44819,7 @@
         "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
@@ -44896,6 +44915,7 @@
         "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
@@ -68775,6 +68795,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -70355,7 +70376,8 @@
             "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?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
+        "supports_system_messages": true
     },
     "azure/eu/o3-2025-04-16": {
         "deprecation_date": "2026-11-19",
@@ -70373,7 +70395,8 @@
             "search_context_size_low": 0.014,
             "search_context_size_medium": 0.014
         },
-        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'"
+        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
+        "supports_system_messages": true
     },
     "azure/eu/o3-deep-research": {
         "deprecation_date": "2026-11-19",
@@ -70400,7 +70423,8 @@
             "search_context_size_low": 0.014,
             "search_context_size_medium": 0.014
         },
-        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'"
+        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
+        "supports_system_messages": true
     },
     "azure/eu/o4-mini-2025-04-16": {
         "deprecation_date": "2026-11-19",
@@ -70418,7 +70442,8 @@
             "search_context_size_low": 0.014,
             "search_context_size_medium": 0.014
         },
-        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'"
+        "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
+        "supports_system_messages": true
     },
     "azure/eu/text-embedding-3-large": {
         "deprecation_date": "2028-02-09",
diff --git a/model_prices_and_context_window.json b/model_prices_and_context_window.json
index c6bbb63b6fc..5fb0ab11873 100644
--- a/model_prices_and_context_window.json
+++ b/model_prices_and_context_window.json
@@ -5359,6 +5359,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$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
     },
@@ -5376,6 +5377,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
         "supports_prompt_caching": true,
         "supports_reasoning": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -11330,6 +11332,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -11367,6 +11370,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -11419,6 +11423,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -11436,6 +11441,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$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
     },
@@ -11540,6 +11546,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -11565,6 +11572,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12267,6 +12275,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12304,6 +12313,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12321,6 +12331,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$filter=serviceName%20eq%20'Foundry%20Models'%20and%20armRegionName%20eq%20'eastus'%20and%20priceType%20eq%20'Consumption'",
         "supports_prompt_caching": true,
         "supports_reasoning": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -12338,6 +12349,7 @@
         "source": "https://prices.azure.com/api/retail/prices?$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
     },
@@ -12363,6 +12375,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -12388,6 +12401,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": true
     },
@@ -44525,6 +44539,7 @@
         "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
@@ -44640,6 +44655,7 @@
         "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
@@ -44661,6 +44677,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -44681,6 +44698,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -44801,6 +44819,7 @@
         "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
@@ -44896,6 +44915,7 @@
         "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
@@ -68775,6 +68795,7 @@
         "supports_prompt_caching": true,
         "supports_reasoning": true,
         "supports_response_schema": true,
+        "supports_system_messages": true,
         "supports_tool_choice": true,
         "supports_vision": false
     },
@@ -70355,7 +70376,8 @@
             "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",
@@ -70373,7 +70395,8 @@
             "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",
@@ -70400,7 +70423,8 @@
             "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",
@@ -70418,7 +70442,8 @@
             "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 e78e1a6f12b..ca96b75ef87 100644
--- a/tests/unit/llms/openai/test_o_series_transformation.py
+++ b/tests/unit/llms/openai/test_o_series_transformation.py
@@ -5,6 +5,7 @@ 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
 
@@ -198,3 +199,24 @@ def test_translate_developer_role_keeps_developer_messages_untouched() -> None:
         )
         == messages
     )
+
+
+@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