diff --git a/tests/entrypoints/anthropic/test_anthropic_messages_conversion.py b/tests/entrypoints/anthropic/test_anthropic_messages_conversion.py
index eb9798980f06..ad9fed1d355a 100644
--- a/tests/entrypoints/anthropic/test_anthropic_messages_conversion.py
+++ b/tests/entrypoints/anthropic/test_anthropic_messages_conversion.py
@@ -635,3 +635,143 @@ def test_redacted_thinking_block_is_accepted(self):
         # Redacted thinking is ignored, normal thinking still becomes reasoning.
         assert asst.get("reasoning") == "Thinking..."
         assert asst.get("content") == "Hi!"
+
+
+class TestInlineSystemMessageInMessagesArray:
+    """Verify that ``role: system`` messages embedded inside the ``messages``
+    array are accepted and merged with the top-level ``system`` prompt.
+
+    This handles clients that place system messages inside the messages array
+    instead of the Anthropic-standard top-level ``system`` field.
+    """
+
+    def test_inline_system_merged_with_top_level_system(self):
+        """Full integration: inline system + top-level system + user message."""
+        request = _make_request(
+            [
+                {
+                    "role": "user",
+                    "content": [
+                        {
+                            "type": "text",
+                            "text": "<system-reminder>\n.....\n</system-reminder>\n\n",
+                        },
+                        {
+                            "type": "text",
+                            "text": "help?",
+                            "cache_control": {"type": "ephemeral"},
+                        },
+                    ],
+                },
+                {
+                    "role": "system",
+                    "content": ".....",
+                },
+            ],
+            system=[
+                {
+                    "type": "text",
+                    "text": "x-anthropic-billing-header: "
+                    "cc_version=2.1.160.bca; cc_entrypoint=cli; cch=d1d48;",
+                },
+                {
+                    "type": "text",
+                    "text": "You are Claude Code, Anthropic's official CLI for Claude.",
+                    "cache_control": {"type": "ephemeral"},
+                },
+                {
+                    "type": "text",
+                    "text": "....",
+                    "cache_control": {"type": "ephemeral"},
+                },
+            ],
+            tools=[],
+        )
+
+        result = _convert(request)
+
+        # First message should be the merged system prompt.
+        assert result.messages[0]["role"] == "system"
+        # Billing header stripped, inline system appended.
+        assert (
+            result.messages[0]["content"]
+            == "You are Claude Code, Anthropic's official CLI for Claude."
+            "...."
+            "....."
+        )
+
+        # Second message should be the user message, content preserved.
+        assert result.messages[1]["role"] == "user"
+        user_content = result.messages[1]["content"]
+        assert len(user_content) == 2
+        assert user_content[0] == {
+            "type": "text",
+            "text": "<system-reminder>\n.....\n</system-reminder>\n\n",
+        }
+        assert user_content[1] == {
+            "type": "text",
+            "text": "help?",
+        }
+
+    def test_inline_system_string_only(self):
+        """Only an inline system string, no top-level system."""
+        request = _make_request(
+            [
+                {"role": "user", "content": "Hello"},
+                {"role": "system", "content": "Be concise."},
+            ]
+        )
+        result = _convert(request)
+
+        assert result.messages[0]["role"] == "system"
+        assert result.messages[0]["content"] == "Be concise."
+        assert result.messages[1]["role"] == "user"
+
+    def test_inline_system_list_content(self):
+        """Inline system with list content blocks."""
+        request = _make_request(
+            [
+                {"role": "user", "content": "Hi"},
+                {
+                    "role": "system",
+                    "content": [
+                        {"type": "text", "text": "Part one. "},
+                        {"type": "text", "text": "Part two."},
+                    ],
+                },
+            ]
+        )
+        result = _convert(request)
+
+        assert result.messages[0]["role"] == "system"
+        assert result.messages[0]["content"] == "Part one. Part two."
+
+    def test_multiple_inline_system_messages(self):
+        """Multiple inline system messages should all be merged."""
+        request = _make_request(
+            [
+                {"role": "system", "content": "First system."},
+                {"role": "user", "content": "Hello"},
+                {"role": "system", "content": "Second system."},
+            ]
+        )
+        result = _convert(request)
+
+        assert result.messages[0]["role"] == "system"
+        assert result.messages[0]["content"] == "First system.Second system."
+        assert result.messages[1]["role"] == "user"
+
+    def test_inline_system_with_top_level_string(self):
+        """Top-level system is a string, inline system is also present."""
+        request = _make_request(
+            [
+                {"role": "user", "content": "Hello"},
+                {"role": "system", "content": "Inline hint."},
+            ],
+            system="Top-level prompt.",
+        )
+        result = _convert(request)
+
+        assert result.messages[0]["role"] == "system"
+        assert result.messages[0]["content"] == "Top-level prompt.Inline hint."
+        assert result.messages[1]["role"] == "user"
diff --git a/vllm/entrypoints/anthropic/protocol.py b/vllm/entrypoints/anthropic/protocol.py
index 3ebc171173e9..279f36253455 100644
--- a/vllm/entrypoints/anthropic/protocol.py
+++ b/vllm/entrypoints/anthropic/protocol.py
@@ -65,7 +65,7 @@ class AnthropicContentBlock(BaseModel):
 class AnthropicMessage(BaseModel):
     """Message structure"""
 
-    role: Literal["user", "assistant"]
+    role: Literal["user", "assistant", "system"]
     content: str | list[AnthropicContentBlock]
 
 
diff --git a/vllm/entrypoints/anthropic/serving.py b/vllm/entrypoints/anthropic/serving.py
index 915cee59f981..2bdec6f4ec33 100644
--- a/vllm/entrypoints/anthropic/serving.py
+++ b/vllm/entrypoints/anthropic/serving.py
@@ -143,23 +143,36 @@ def _convert_system_message(
         openai_messages: list[dict[str, Any]],
     ) -> None:
         """Convert Anthropic system message to OpenAI format"""
-        if not anthropic_request.system:
-            return
+        system_parts: list[str] = []
 
-        if isinstance(anthropic_request.system, str):
-            openai_messages.append(
-                {"role": "system", "content": anthropic_request.system}
-            )
-        else:
-            system_prompt = ""
-            for block in anthropic_request.system:
-                if block.type == "text" and block.text:
-                    # Strip Claude Code's attribution header which contains
-                    # a per-request hash that defeats prefix caching.
-                    if block.text.startswith("x-anthropic-billing-header"):
-                        continue
-                    system_prompt += block.text
-            openai_messages.append({"role": "system", "content": system_prompt})
+        # Top-level system field
+        if anthropic_request.system:
+            if isinstance(anthropic_request.system, str):
+                system_parts.append(anthropic_request.system)
+            else:
+                for block in anthropic_request.system:
+                    if block.type == "text" and block.text:
+                        # Strip Claude Code's attribution header which contains
+                        # a per-request hash that defeats prefix caching.
+                        if block.text.startswith("x-anthropic-billing-header"):
+                            continue
+                        system_parts.append(block.text)
+
+        # System messages embedded inside the messages array
+        for msg in anthropic_request.messages:
+            if msg.role != "system":
+                continue
+            if isinstance(msg.content, str):
+                system_parts.append(msg.content)
+            else:
+                for block in msg.content:
+                    if block.type == "text" and block.text:
+                        if block.text.startswith("x-anthropic-billing-header"):
+                            continue
+                        system_parts.append(block.text)
+
+        if system_parts:
+            openai_messages.append({"role": "system", "content": "".join(system_parts)})
 
     @classmethod
     def _convert_messages(
@@ -167,6 +180,9 @@ def _convert_messages(
     ) -> None:
         """Convert Anthropic messages to OpenAI format"""
         for msg in messages:
+            if msg.role == "system":
+                continue
+
             openai_msg: dict[str, Any] = {"role": msg.role}  # type: ignore
 
             if isinstance(msg.content, str):