diff --git a/pyrit/prompt_target/azure_ml_chat_target.py b/pyrit/prompt_target/azure_ml_chat_target.py
index cc83332027..4795d42d0d 100644
--- a/pyrit/prompt_target/azure_ml_chat_target.py
+++ b/pyrit/prompt_target/azure_ml_chat_target.py
@@ -42,7 +42,10 @@ class AzureMLChatTarget(PromptChatTarget):
     api_key_environment_variable: str = "AZURE_ML_KEY"
 
     _DEFAULT_CAPABILITIES: TargetCapabilities = TargetCapabilities(
-        supports_multi_message_pieces=True, supports_editable_history=True, supports_multi_turn=True
+        supports_multi_message_pieces=True,
+        supports_editable_history=True,
+        supports_multi_turn=True,
+        supports_system_prompt=True,
     )
 
     def __init__(
diff --git a/pyrit/prompt_target/common/prompt_chat_target.py b/pyrit/prompt_target/common/prompt_chat_target.py
index af12a11a1e..6b77ac03b1 100644
--- a/pyrit/prompt_target/common/prompt_chat_target.py
+++ b/pyrit/prompt_target/common/prompt_chat_target.py
@@ -22,7 +22,9 @@ class PromptChatTarget(PromptTarget):
     """
 
     _DEFAULT_CAPABILITIES: TargetCapabilities = TargetCapabilities(
-        supports_multi_turn=True, supports_multi_message_pieces=True
+        supports_multi_turn=True,
+        supports_multi_message_pieces=True,
+        supports_system_prompt=True,
     )
 
     def __init__(
diff --git a/pyrit/prompt_target/common/target_capabilities.py b/pyrit/prompt_target/common/target_capabilities.py
index 5b1b596120..e6ced6a1a2 100644
--- a/pyrit/prompt_target/common/target_capabilities.py
+++ b/pyrit/prompt_target/common/target_capabilities.py
@@ -38,6 +38,9 @@ class attribute. Users can override individual capabilities per instance
     # multi-turn interactions and that the attack history is not immutable once set.
     supports_editable_history: bool = False
 
+    # Whether the target natively supports system prompts.
+    supports_system_prompt: bool = False
+
     # The input modalities supported by the target (e.g., "text", "image").
     input_modalities: frozenset[frozenset[PromptDataType]] = frozenset({frozenset(["text"])})
 
@@ -76,6 +79,7 @@ def get_known_capabilities(underlying_model: str) -> "Optional[TargetCapabilitie
 _GPT_4O = TargetCapabilities(
     supports_multi_turn=True,
     supports_multi_message_pieces=True,
+    supports_system_prompt=True,
     supports_json_output=True,
     input_modalities=_TEXT_IMAGE_INPUT,
     output_modalities=_TEXT_OUTPUT,
@@ -84,6 +88,7 @@ def get_known_capabilities(underlying_model: str) -> "Optional[TargetCapabilitie
 _GPT_5 = TargetCapabilities(
     supports_multi_turn=True,
     supports_multi_message_pieces=True,
+    supports_system_prompt=True,
     supports_json_schema=True,
     supports_json_output=True,
     input_modalities=_TEXT_IMAGE_INPUT,
diff --git a/pyrit/prompt_target/hugging_face/hugging_face_chat_target.py b/pyrit/prompt_target/hugging_face/hugging_face_chat_target.py
index 8eeb0bfc6a..13152af775 100644
--- a/pyrit/prompt_target/hugging_face/hugging_face_chat_target.py
+++ b/pyrit/prompt_target/hugging_face/hugging_face_chat_target.py
@@ -33,7 +33,9 @@ class HuggingFaceChatTarget(PromptChatTarget):
     """
 
     _DEFAULT_CAPABILITIES: TargetCapabilities = TargetCapabilities(
-        supports_multi_turn=True, supports_editable_history=True
+        supports_multi_turn=True,
+        supports_editable_history=True,
+        supports_system_prompt=True,
     )
 
     # Class-level cache for model and tokenizer
diff --git a/pyrit/prompt_target/openai/openai_chat_target.py b/pyrit/prompt_target/openai/openai_chat_target.py
index dcc7409934..ba0abf7cfa 100644
--- a/pyrit/prompt_target/openai/openai_chat_target.py
+++ b/pyrit/prompt_target/openai/openai_chat_target.py
@@ -69,6 +69,7 @@ class OpenAIChatTarget(OpenAITarget, PromptChatTarget):
         supports_multi_turn=True,
         supports_json_output=True,
         supports_multi_message_pieces=True,
+        supports_system_prompt=True,
     )
 
     def __init__(
diff --git a/pyrit/prompt_target/openai/openai_realtime_target.py b/pyrit/prompt_target/openai/openai_realtime_target.py
index 22edf20391..ffc8d7a2ca 100644
--- a/pyrit/prompt_target/openai/openai_realtime_target.py
+++ b/pyrit/prompt_target/openai/openai_realtime_target.py
@@ -71,6 +71,7 @@ class RealtimeTarget(OpenAITarget, PromptChatTarget):
     _DEFAULT_CAPABILITIES: TargetCapabilities = TargetCapabilities(
         supports_multi_turn=True,
         supports_multi_message_pieces=True,
+        supports_system_prompt=True,
         input_modalities=frozenset(
             {
                 frozenset(["text"]),
diff --git a/pyrit/prompt_target/openai/openai_response_target.py b/pyrit/prompt_target/openai/openai_response_target.py
index be720fa5c9..b41b40a30f 100644
--- a/pyrit/prompt_target/openai/openai_response_target.py
+++ b/pyrit/prompt_target/openai/openai_response_target.py
@@ -72,6 +72,7 @@ class OpenAIResponseTarget(OpenAITarget, PromptChatTarget):
         supports_multi_turn=True,
         supports_json_output=True,
         supports_multi_message_pieces=True,
+        supports_system_prompt=True,
         input_modalities=frozenset(
             {
                 frozenset(["text"]),
diff --git a/tests/unit/target/test_target_capabilities.py b/tests/unit/target/test_target_capabilities.py
index f64d7d3203..48b62297c3 100644
--- a/tests/unit/target/test_target_capabilities.py
+++ b/tests/unit/target/test_target_capabilities.py
@@ -243,6 +243,7 @@ def test_hugging_face_chat_target_capabilities(self):
         caps = HuggingFaceChatTarget._DEFAULT_CAPABILITIES
         assert caps.supports_editable_history is True
         assert caps.supports_multi_turn is True
+        assert caps.supports_system_prompt is True
 
     def test_azure_ml_chat_target_capabilities(self):
         from pyrit.prompt_target import AzureMLChatTarget
@@ -253,6 +254,31 @@ def test_azure_ml_chat_target_capabilities(self):
         )
         assert target.capabilities.supports_editable_history is True
         assert target.capabilities.supports_multi_message_pieces is True
+        assert target.capabilities.supports_system_prompt is True
+
+    @patch.dict("os.environ", _CLEAN_UNDERLYING_MODEL_ENV)
+    def test_prompt_chat_targets_support_system_prompt(self):
+        from pyrit.prompt_target import OpenAIChatTarget, OpenAIResponseTarget, RealtimeTarget
+
+        openai_chat_target = OpenAIChatTarget(
+            model_name="test-model",
+            endpoint="https://mock.azure.com/",
+            api_key="mock-api-key",
+        )
+        openai_response_target = OpenAIResponseTarget(
+            model_name="o1",
+            endpoint="https://mock.azure.com/",
+            api_key="mock-api-key",
+        )
+        realtime_target = RealtimeTarget(
+            model_name="gpt-4o-realtime",
+            endpoint="https://mock.azure.com/",
+            api_key="mock-api-key",
+        )
+
+        assert openai_chat_target.capabilities.supports_system_prompt is True
+        assert openai_response_target.capabilities.supports_system_prompt is True
+        assert realtime_target.capabilities.supports_system_prompt is True
 
     def test_custom_capabilities_override_modalities(self):
         from pyrit.prompt_target import OpenAIChatTarget, TargetCapabilities
@@ -415,3 +441,12 @@ def test_recognized_model_overrides_class_default(self):
         cls = self._make_target_class(default_caps=minimal_caps)
         result = cls.get_default_capabilities("tts")
         assert result.output_modalities == frozenset({frozenset(["audio_path"])})
+
+    def test_prompt_chat_target_preserves_system_prompt_for_recognized_model(self):
+        from pyrit.prompt_target.common.prompt_chat_target import PromptChatTarget
+
+        result = PromptChatTarget.get_default_capabilities("gpt-4o")
+
+        assert result.supports_multi_turn is True
+        assert result.supports_multi_message_pieces is True
+        assert result.supports_system_prompt is True