diff --git a/tests/renderers/test_hf.py b/tests/renderers/test_hf.py
index c2eb6556394..0545457eb7a 100644
--- a/tests/renderers/test_hf.py
+++ b/tests/renderers/test_hf.py
@@ -7,6 +7,9 @@ from vllm.config import ModelConfig
 from vllm.entrypoints.chat_utils import load_chat_template
 from vllm.entrypoints.openai.chat_completion.protocol import ChatCompletionRequest
 from vllm.renderers.hf import (
+    _consolidate_system_messages,
+    _convert_developer_to_system,
+    _detect_developer_role_support,
     _get_hf_base_chat_template_params,
     _try_extract_ast,
     resolve_chat_template,
@@ -592,3 +595,322 @@ def test_get_gen_prompt(
         f"The generated prompt does not match the expected output for "
         f"model {model} and template {template}"
     )
+
+
+class TestConvertDeveloperToSystem:
+    def test_converts_role(self):
+        conversation = [
+            {"role": "developer", "content": "You are helpful."},
+            {"role": "user", "content": "Hello"},
+        ]
+        result = _convert_developer_to_system(conversation)
+        assert result[0]["role"] == "system"
+        assert result[0]["content"] == "You are helpful."
+        assert result[1]["role"] == "user"
+
+    def test_removes_tools_key(self):
+        conversation = [
+            {
+                "role": "developer",
+                "content": "Instructions",
+                "tools": [{"type": "function"}],
+            },
+        ]
+        result = _convert_developer_to_system(conversation)
+        assert "tools" not in result[0]
+
+    def test_no_developer_messages_unchanged(self):
+        conversation = [
+            {"role": "system", "content": "System prompt"},
+            {"role": "user", "content": "Hello"},
+        ]
+        result = _convert_developer_to_system(conversation)
+        assert result[0]["role"] == "system"
+        assert result[1]["role"] == "user"
+
+    def test_does_not_mutate_original(self):
+        original = {
+            "role": "developer",
+            "content": "Instructions",
+            "tools": [{"type": "function"}],
+        }
+        conversation = [original]
+        _convert_developer_to_system(conversation)
+        assert original["role"] == "developer"
+        assert "tools" in original
+
+
+# --- Developer role detection and conversion tests ---
+
+CHATML_TEMPLATE = (
+    "{% for message in messages %}"
+    "{{'<|im_start|>' + message['role'] + '\\n' + message['content']}}"
+    "{% if (loop.last and add_generation_prompt) or not loop.last %}"
+    "{{ '<|im_end|>' + '\\n'}}"
+    "{% endif %}"
+    "{% endfor %}"
+    "{% if add_generation_prompt and messages[-1]['role'] != 'assistant' %}"
+    "{{ '<|im_start|>assistant\\n' }}"
+    "{% endif %}"
+)
+
+TEMPLATE_WITH_DEVELOPER = (
+    "{% for message in messages %}"
+    "{% if message['role'] == 'developer' %}"
+    "{{'<|im_start|>developer\\n' + message['content'] + '<|im_end|>\\n'}}"
+    "{% elif message['role'] == 'system' %}"
+    "{{'<|im_start|>system\\n' + message['content'] + '<|im_end|>\\n'}}"
+    "{% elif message['role'] == 'user' %}"
+    "{{'<|im_start|>user\\n' + message['content'] + '<|im_end|>\\n'}}"
+    "{% elif message['role'] == 'assistant' %}"
+    "{{'<|im_start|>assistant\\n' + message['content'] + '<|im_end|>\\n'}}"
+    "{% endif %}"
+    "{% endfor %}"
+    "{% if add_generation_prompt %}"
+    "{{ '<|im_start|>assistant\\n' }}"
+    "{% endif %}"
+)
+
+STRICT_ROLE_TEMPLATE = (
+    "{% for message in messages %}"
+    "{% if message['role'] == 'system' %}"
+    "{{'<|im_start|>system\\n' + message['content'] + '<|im_end|>\\n'}}"
+    "{% elif message['role'] == 'user' %}"
+    "{{'<|im_start|>user\\n' + message['content'] + '<|im_end|>\\n'}}"
+    "{% elif message['role'] == 'assistant' %}"
+    "{{'<|im_start|>assistant\\n' + message['content'] + '<|im_end|>\\n'}}"
+    "{% else %}"
+    "{{ raise_exception('Unexpected message role: ' + message['role']) }}"
+    "{% endif %}"
+    "{% endfor %}"
+    "{% if add_generation_prompt %}"
+    "{{ '<|im_start|>assistant\\n' }}"
+    "{% endif %}"
+)
+
+
+class TestDetectDeveloperRoleSupport:
+    def test_absent_in_chatml(self):
+        assert _detect_developer_role_support(CHATML_TEMPLATE) is False
+
+    def test_present_double_quotes(self):
+        assert _detect_developer_role_support(TEMPLATE_WITH_DEVELOPER) is True
+
+    def test_present_single_quotes(self):
+        template = TEMPLATE_WITH_DEVELOPER.replace('"developer"', "'developer'")
+        assert _detect_developer_role_support(template) is True
+
+    def test_absent_in_strict_template(self):
+        assert _detect_developer_role_support(STRICT_ROLE_TEMPLATE) is False
+
+
+class TestSafeApplyChatTemplateDeveloperRole:
+    @pytest.fixture
+    def model_config(self):
+        return ModelConfig(
+            "facebook/opt-125m",
+            tokenizer="facebook/opt-125m",
+            tokenizer_mode="auto",
+            trust_remote_code=False,
+            dtype="float16",
+        )
+
+    @pytest.fixture
+    def tokenizer(self):
+        return get_tokenizer("facebook/opt-125m")
+
+    def test_developer_converted_to_system_for_chatml(self, model_config, tokenizer):
+        conversation = [
+            {"role": "developer", "content": "You are a helpful assistant."},
+            {"role": "user", "content": "Hello"},
+        ]
+        result = safe_apply_chat_template(
+            model_config,
+            tokenizer,
+            conversation,
+            chat_template=CHATML_TEMPLATE,
+            tokenize=False,
+            add_generation_prompt=True,
+        )
+        assert "<|im_start|>system" in result
+        assert "You are a helpful assistant." in result
+        assert "<|im_start|>developer" not in result
+
+    def test_developer_preserved_when_template_supports_it(
+        self, model_config, tokenizer
+    ):
+        conversation = [
+            {"role": "developer", "content": "You are a helpful assistant."},
+            {"role": "user", "content": "Hello"},
+        ]
+        result = safe_apply_chat_template(
+            model_config,
+            tokenizer,
+            conversation,
+            chat_template=TEMPLATE_WITH_DEVELOPER,
+            tokenize=False,
+            add_generation_prompt=True,
+        )
+        assert "<|im_start|>developer" in result
+        assert "You are a helpful assistant." in result
+
+    def test_developer_does_not_crash_strict_template(self, model_config, tokenizer):
+        conversation = [
+            {"role": "developer", "content": "You are a helpful assistant."},
+            {"role": "user", "content": "Hello"},
+        ]
+        result = safe_apply_chat_template(
+            model_config,
+            tokenizer,
+            conversation,
+            chat_template=STRICT_ROLE_TEMPLATE,
+            tokenize=False,
+            add_generation_prompt=True,
+        )
+        assert "<|im_start|>system" in result
+        assert "You are a helpful assistant." in result
+
+    def test_no_developer_messages_no_overhead(self, model_config, tokenizer):
+        conversation = [
+            {"role": "system", "content": "You are helpful."},
+            {"role": "user", "content": "Hello"},
+        ]
+        result = safe_apply_chat_template(
+            model_config,
+            tokenizer,
+            conversation,
+            chat_template=CHATML_TEMPLATE,
+            tokenize=False,
+            add_generation_prompt=True,
+        )
+        assert "<|im_start|>system" in result
+        assert "You are helpful." in result
+
+    def test_developer_at_non_first_position_consolidated(
+        self, model_config, tokenizer
+    ):
+        conversation = [
+            {"role": "system", "content": "You are helpful."},
+            {"role": "user", "content": "Hello"},
+            {"role": "assistant", "content": "Hi there!"},
+            {"role": "developer", "content": "Be concise."},
+            {"role": "user", "content": "What is 2+2?"},
+        ]
+        result = safe_apply_chat_template(
+            model_config,
+            tokenizer,
+            conversation,
+            chat_template=SYSTEM_FIRST_TEMPLATE,
+            tokenize=False,
+            add_generation_prompt=True,
+        )
+        assert "<|im_start|>system" in result
+        assert "You are helpful." in result
+        assert "Be concise." in result
+        assert "What is 2+2?" in result
+
+    def test_developer_only_no_prior_system(self, model_config, tokenizer):
+        conversation = [
+            {"role": "user", "content": "Hello"},
+            {"role": "developer", "content": "Be concise."},
+            {"role": "user", "content": "What is 2+2?"},
+        ]
+        result = safe_apply_chat_template(
+            model_config,
+            tokenizer,
+            conversation,
+            chat_template=SYSTEM_FIRST_TEMPLATE,
+            tokenize=False,
+            add_generation_prompt=True,
+        )
+        assert "<|im_start|>system" in result
+        assert "Be concise." in result
+
+
+SYSTEM_FIRST_TEMPLATE = (
+    "{% for message in messages %}"
+    "{% if message['role'] == 'system' %}"
+    "{% if not loop.first %}"
+    "{{ raise_exception('System message must be at the beginning.') }}"
+    "{% endif %}"
+    "{{'<|im_start|>system\\n' + message['content'] + '<|im_end|>\\n'}}"
+    "{% elif message['role'] == 'user' %}"
+    "{{'<|im_start|>user\\n' + message['content'] + '<|im_end|>\\n'}}"
+    "{% elif message['role'] == 'assistant' %}"
+    "{{'<|im_start|>assistant\\n' + message['content'] + '<|im_end|>\\n'}}"
+    "{% else %}"
+    "{{ raise_exception('Unexpected message role: ' + message['role']) }}"
+    "{% endif %}"
+    "{% endfor %}"
+    "{% if add_generation_prompt %}"
+    "{{ '<|im_start|>assistant\\n' }}"
+    "{% endif %}"
+)
+
+
+class TestConsolidateSystemMessages:
+    def test_no_system_messages_unchanged(self):
+        conversation = [
+            {"role": "user", "content": "Hello"},
+            {"role": "assistant", "content": "Hi"},
+        ]
+        result = _consolidate_system_messages(conversation)
+        assert result == conversation
+
+    def test_single_system_at_start_unchanged(self):
+        conversation = [
+            {"role": "system", "content": "You are helpful."},
+            {"role": "user", "content": "Hello"},
+        ]
+        result = _consolidate_system_messages(conversation)
+        assert result == conversation
+
+    def test_system_at_non_first_position_moved(self):
+        conversation = [
+            {"role": "user", "content": "Hello"},
+            {"role": "system", "content": "You are helpful."},
+        ]
+        result = _consolidate_system_messages(conversation)
+        assert result[0]["role"] == "system"
+        assert result[0]["content"] == "You are helpful."
+        assert result[1]["role"] == "user"
+        assert result[1]["content"] == "Hello"
+
+    def test_multiple_system_messages_merged(self):
+        conversation = [
+            {"role": "system", "content": "You are helpful."},
+            {"role": "user", "content": "Hello"},
+            {"role": "system", "content": "Be concise."},
+        ]
+        result = _consolidate_system_messages(conversation)
+        assert len(result) == 2
+        assert result[0]["role"] == "system"
+        assert result[0]["content"] == "You are helpful.\n\nBe concise."
+        assert result[1]["role"] == "user"
+
+    def test_list_content_handled(self):
+        conversation = [
+            {"role": "user", "content": "Hello"},
+            {
+                "role": "system",
+                "content": [
+                    {"type": "text", "text": "Rule 1."},
+                    {"type": "text", "text": "Rule 2."},
+                ],
+            },
+        ]
+        result = _consolidate_system_messages(conversation)
+        assert result[0]["role"] == "system"
+        assert result[0]["content"] == "Rule 1.\nRule 2."
+        assert result[1]["role"] == "user"
+
+    def test_does_not_mutate_original(self):
+        conversation = [
+            {"role": "user", "content": "Hello"},
+            {"role": "system", "content": "You are helpful."},
+        ]
+        original_len = len(conversation)
+        _consolidate_system_messages(conversation)
+        assert len(conversation) == original_len
+        assert conversation[0]["role"] == "user"
+        assert conversation[1]["role"] == "system"
diff --git a/vllm/renderers/hf.py b/vllm/renderers/hf.py
index e796607722a..e57d0586aa0 100644
--- a/vllm/renderers/hf.py
+++ b/vllm/renderers/hf.py
@@ -450,6 +450,66 @@ def _detect_content_format(
         return "openai"
 
 
+@lru_cache(maxsize=32)
+def _detect_developer_role_support(chat_template: str) -> bool:
+    return '"developer"' in chat_template or "'developer'" in chat_template
+
+
+def _convert_developer_to_system(
+    conversation: list[ConversationMessage],
+) -> list[ConversationMessage]:
+    converted: list[ConversationMessage] = []
+    for msg in conversation:
+        if msg["role"] == "developer":
+            new_msg = dict(msg)
+            new_msg["role"] = "system"
+            new_msg.pop("tools", None)
+            converted.append(new_msg)  # type: ignore[arg-type]
+        else:
+            converted.append(msg)
+    return converted
+
+
+def _consolidate_system_messages(
+    conversation: list[ConversationMessage],
+) -> list[ConversationMessage]:
+    """Merge all system messages into one at position 0.
+
+    Some chat templates (e.g. Qwen 3.6) require the system message to be the
+    very first message.  After developer-to-system conversion, system messages
+    may appear at non-first positions; this merges them into a single message.
+    """
+    system_contents: list[str] = []
+    non_system: list[ConversationMessage] = []
+    needs_consolidation = False
+    for i, msg in enumerate(conversation):
+        if msg["role"] == "system":
+            if i > 0 or system_contents:
+                needs_consolidation = True
+            content = msg.get("content", "")
+            if isinstance(content, list):
+                parts = []
+                for part in content:
+                    if isinstance(part, dict) and "text" in part:
+                        parts.append(part["text"])
+                    elif isinstance(part, str):
+                        parts.append(part)
+                content = "\n".join(parts)
+            if content:
+                system_contents.append(content)
+        else:
+            non_system.append(msg)
+
+    if not needs_consolidation:
+        return conversation
+
+    merged: ConversationMessage = {
+        "role": "system",
+        "content": "\n\n".join(system_contents),
+    }
+    return [merged, *non_system]
+
+
 def _resolve_chat_template_content_format(
     chat_template: str | None,
     tools: list[dict[str, Any]] | None,
@@ -653,7 +713,15 @@ def safe_apply_chat_template(
             "allowed, so you must provide a chat template if the tokenizer "
             "does not define one."
         )
-
+    if any(
+        msg["role"] == "developer" for msg in conversation
+    ) and not _detect_developer_role_support(chat_template):
+        conversation = _convert_developer_to_system(conversation)
+        conversation = _consolidate_system_messages(conversation)
+        logger.info_once(
+            "Chat template does not support the 'developer' message role. "
+            "Converting developer messages to 'system' role.",
+        )
     resolved_kwargs = resolve_chat_template_kwargs(
         tokenizer=tokenizer,
         chat_template=chat_template,