diff --git a/tests/utils/test_chat_template_on_cpu.py b/tests/utils/test_chat_template_on_cpu.py
new file mode 100644
index 00000000000..66434ef7d86
--- /dev/null
+++ b/tests/utils/test_chat_template_on_cpu.py
@@ -0,0 +1,126 @@
+# Copyright 2026 Bytedance Ltd. and/or its affiliates
+
+import pytest
+
+from verl.utils.chat_template import extract_system_prompt_and_generation, initialize_system_prompt
+
+
+class AppendOnlyTokenizer:
+    prefix = [1, 2]
+    user_turn = [10, 11]
+    assistant_turn = [20]
+    generation_prompt = [30]
+
+    def apply_chat_template(self, messages, *, add_generation_prompt, tokenize, **kwargs):
+        assert tokenize
+        token_ids = list(self.prefix)
+        for message in messages:
+            if message["role"] == "user":
+                token_ids.extend(self.user_turn)
+            elif message["role"] == "assistant":
+                token_ids.extend(self.assistant_turn)
+            else:
+                raise ValueError(f"Unsupported role: {message['role']}")
+
+        if add_generation_prompt:
+            token_ids.extend(self.generation_prompt)
+        return token_ids
+
+
+class AlternatingTokenizer(AppendOnlyTokenizer):
+    prefix = [101]
+    user_turn = [110]
+    assistant_turn = [120]
+
+    def apply_chat_template(self, messages, *, add_generation_prompt, tokenize, **kwargs):
+        for prev_message, message in zip(messages, messages[1:], strict=False):
+            if prev_message["role"] == message["role"]:
+                raise ValueError("Conversation roles must alternate")
+        return super().apply_chat_template(
+            messages,
+            add_generation_prompt=add_generation_prompt,
+            tokenize=tokenize,
+            **kwargs,
+        )
+
+
+class AppendOnlyWithFinalTokenTokenizer(AppendOnlyTokenizer):
+    final_token = [99]
+
+    def apply_chat_template(self, messages, *, add_generation_prompt, tokenize, **kwargs):
+        token_ids = super().apply_chat_template(
+            messages,
+            add_generation_prompt=False,
+            tokenize=tokenize,
+            **kwargs,
+        )
+        if add_generation_prompt:
+            token_ids.extend(self.generation_prompt)
+        else:
+            token_ids.extend(self.final_token)
+        return token_ids
+
+
+class ConversationFinalTokenTokenizer:
+    user_turn = [210, 211]
+    assistant_turn = [220, 221]
+    final_token = [299]
+    generation_prompt = [230]
+
+    def apply_chat_template(self, messages, *, add_generation_prompt, tokenize, **kwargs):
+        assert tokenize
+        token_ids = []
+        for message in messages:
+            if message["role"] == "user":
+                token_ids.extend(self.user_turn)
+            elif message["role"] == "assistant":
+                token_ids.extend(self.assistant_turn)
+            else:
+                raise ValueError(f"Unsupported role: {message['role']}")
+
+        if add_generation_prompt:
+            token_ids.extend(self.generation_prompt)
+        else:
+            token_ids.extend(self.final_token)
+        return token_ids
+
+
+def test_initialize_system_prompt_infers_append_only_prefix():
+    assert initialize_system_prompt(AppendOnlyTokenizer()) == AppendOnlyTokenizer.prefix
+
+
+def test_extract_system_prompt_and_generation_uses_append_only_prefix():
+    system_prompt, generation_prompt = extract_system_prompt_and_generation(AppendOnlyTokenizer())
+
+    assert system_prompt == AppendOnlyTokenizer.prefix
+    assert generation_prompt == AppendOnlyTokenizer.generation_prompt
+
+
+def test_initialize_system_prompt_supports_alternating_role_templates():
+    assert initialize_system_prompt(AlternatingTokenizer()) == AlternatingTokenizer.prefix
+
+
+def test_initialize_system_prompt_handles_common_final_tokens():
+    assert initialize_system_prompt(AppendOnlyWithFinalTokenTokenizer()) == AppendOnlyWithFinalTokenTokenizer.prefix
+
+
+@pytest.mark.parametrize("tokenizer_cls", [AppendOnlyWithFinalTokenTokenizer, ConversationFinalTokenTokenizer])
+def test_extract_generation_prompt_handles_replaced_final_tokens(tokenizer_cls):
+    _, generation_prompt = extract_system_prompt_and_generation(tokenizer_cls())
+
+    assert generation_prompt == tokenizer_cls.generation_prompt
+
+
+def test_extract_system_prompt_and_generation_supports_alternating_role_templates():
+    system_prompt, generation_prompt = extract_system_prompt_and_generation(AlternatingTokenizer())
+
+    assert system_prompt == AlternatingTokenizer.prefix
+    assert generation_prompt == AlternatingTokenizer.generation_prompt
+
+
+@pytest.mark.parametrize("helper", [initialize_system_prompt, extract_system_prompt_and_generation])
+def test_system_prompt_inference_ignores_non_append_only_templates(helper):
+    result = helper(ConversationFinalTokenTokenizer())
+    system_prompt = result[0] if isinstance(result, tuple) else result
+
+    assert system_prompt == []
diff --git a/verl/utils/chat_template.py b/verl/utils/chat_template.py
index 7e5a1de3bc5..7a2ca910b4e 100644
--- a/verl/utils/chat_template.py
+++ b/verl/utils/chat_template.py
@@ -10,6 +10,117 @@
 logger.setLevel(os.getenv("VERL_LOGGING_LEVEL", "WARN"))
 
 
+def _apply_chat_template_token_ids(
+    tokenizer, messages: list[dict], *, add_generation_prompt: bool, **kwargs
+) -> list[int]:
+    return normalize_token_ids(
+        tokenizer.apply_chat_template(
+            messages,
+            add_generation_prompt=add_generation_prompt,
+            tokenize=True,
+            **kwargs,
+        )
+    )
+
+
+def _common_suffix_len(*token_lists: list[int]) -> int:
+    suffix_len = 0
+    for tokens in zip(*(reversed(token_ids) for token_ids in token_lists), strict=False):
+        if any(token != tokens[0] for token in tokens[1:]):
+            break
+        suffix_len += 1
+    return suffix_len
+
+
+def _common_prefix_len(first: list[int], second: list[int]) -> int:
+    prefix_len = 0
+    for first_token, second_token in zip(first, second, strict=False):
+        if first_token != second_token:
+            break
+        prefix_len += 1
+    return prefix_len
+
+
+def _remove_suffix(token_ids: list[int], suffix_len: int) -> list[int]:
+    if suffix_len == 0:
+        return token_ids
+    return token_ids[:-suffix_len]
+
+
+def _infer_prefix_from_appended_turn_core(
+    first_turn: list[int], base: list[int], extended: list[int]
+) -> list[int] | None:
+    if len(extended) <= len(base) or extended[: len(base)] != base:
+        return None
+
+    appended_turn = extended[len(base) :]
+    if len(appended_turn) > len(first_turn) or first_turn[-len(appended_turn) :] != appended_turn:
+        return None
+
+    return first_turn[: -len(appended_turn)]
+
+
+def _infer_prefix_from_appended_turn(first_turn: list[int], base: list[int], extended: list[int]) -> list[int] | None:
+    suffix_lens = [0, *range(_common_suffix_len(first_turn, base, extended), 0, -1)]
+    for suffix_len in suffix_lens:
+        system_prompt = _infer_prefix_from_appended_turn_core(
+            _remove_suffix(first_turn, suffix_len),
+            _remove_suffix(base, suffix_len),
+            _remove_suffix(extended, suffix_len),
+        )
+        if system_prompt is not None:
+            return system_prompt
+
+    return None
+
+
+def _extract_generation_prompt(no_generation: list[int], with_generation: list[int]) -> list[int]:
+    prefix_len = _common_prefix_len(no_generation, with_generation)
+    return with_generation[prefix_len:]
+
+
+def _infer_system_prompt(tokenizer, token1: list[int], **apply_chat_template_kwargs) -> list[int]:
+    two_users = [{"role": "user", "content": ""}, {"role": "user", "content": ""}]
+    user_assistant = [{"role": "user", "content": ""}, {"role": "assistant", "content": ""}]
+    user_assistant_user = user_assistant + [{"role": "user", "content": ""}]
+
+    # Prefer the historical consecutive-user probe when the template supports it.
+    try:
+        token2 = _apply_chat_template_token_ids(
+            tokenizer,
+            two_users,
+            add_generation_prompt=False,
+            **apply_chat_template_kwargs,
+        )
+        system_prompt = _infer_prefix_from_appended_turn(token1, token1, token2)
+        if system_prompt is not None:
+            return system_prompt
+    except Exception:
+        logger.debug("Failed to render consecutive user messages for system prompt inference.", exc_info=True)
+
+    # Some official templates require alternating user/assistant roles.
+    try:
+        token2 = _apply_chat_template_token_ids(
+            tokenizer,
+            user_assistant,
+            add_generation_prompt=False,
+            **apply_chat_template_kwargs,
+        )
+        token3 = _apply_chat_template_token_ids(
+            tokenizer,
+            user_assistant_user,
+            add_generation_prompt=False,
+            **apply_chat_template_kwargs,
+        )
+        system_prompt = _infer_prefix_from_appended_turn(token1, token2, token3)
+        if system_prompt is not None:
+            return system_prompt
+    except Exception:
+        logger.debug("Failed to render alternating messages for system prompt inference.", exc_info=True)
+
+    return []
+
+
 def initialize_system_prompt(tokenizer, **apply_chat_template_kwargs) -> list[int]:
     """
     Initialize system prompt tokens for chat templates that support them.
@@ -21,47 +132,32 @@ def initialize_system_prompt(tokenizer, **apply_chat_template_kwargs) -> list[in
     Returns:
         List of token IDs for the system prompt, or empty list if not supported
     """
-    token1 = normalize_token_ids(
-        tokenizer.apply_chat_template(
-            [{"role": "user", "content": ""}], add_generation_prompt=False, tokenize=True, **apply_chat_template_kwargs
-        )
+    token1 = _apply_chat_template_token_ids(
+        tokenizer,
+        [{"role": "user", "content": ""}],
+        add_generation_prompt=False,
+        **apply_chat_template_kwargs,
     )
-    token2 = normalize_token_ids(
-        tokenizer.apply_chat_template(
-            [{"role": "user", "content": ""}] * 2,
-            add_generation_prompt=False,
-            tokenize=True,
-            **apply_chat_template_kwargs,
-        )
-    )
-    # get system prompt tokens
-    system_prompt = token1[: -(len(token2) - len(token1))]
-    return system_prompt
+    return _infer_system_prompt(tokenizer, token1, **apply_chat_template_kwargs)
 
 
 def extract_system_prompt_and_generation(tokenizer, **apply_chat_template_kwargs):
-    token1 = normalize_token_ids(
-        tokenizer.apply_chat_template(
-            [{"role": "user", "content": ""}], add_generation_prompt=False, tokenize=True, **apply_chat_template_kwargs
-        )
-    )
-    token2 = normalize_token_ids(
-        tokenizer.apply_chat_template(
-            [{"role": "user", "content": ""}] * 2,
-            add_generation_prompt=False,
-            tokenize=True,
-            **apply_chat_template_kwargs,
-        )
+    token1 = _apply_chat_template_token_ids(
+        tokenizer,
+        [{"role": "user", "content": ""}],
+        add_generation_prompt=False,
+        **apply_chat_template_kwargs,
     )
     # get system prompt tokens
-    system_prompt = token1[: -(len(token2) - len(token1))]
+    system_prompt = _infer_system_prompt(tokenizer, token1, **apply_chat_template_kwargs)
     # get generate prompt tokens
-    token3 = normalize_token_ids(
-        tokenizer.apply_chat_template(
-            [{"role": "user", "content": ""}], add_generation_prompt=True, tokenize=True, **apply_chat_template_kwargs
-        )
+    token3 = _apply_chat_template_token_ids(
+        tokenizer,
+        [{"role": "user", "content": ""}],
+        add_generation_prompt=True,
+        **apply_chat_template_kwargs,
     )
-    generate_prompt = token3[len(token1) :]
+    generate_prompt = _extract_generation_prompt(token1, token3)
 
     return system_prompt, generate_prompt