diff --git a/tests/entrypoints/pooling/basic/test_encode.py b/tests/entrypoints/pooling/basic/test_encode.py
index ca85d2758f..61222eb780 100644
--- a/tests/entrypoints/pooling/basic/test_encode.py
+++ b/tests/entrypoints/pooling/basic/test_encode.py
@@ -7,6 +7,7 @@ import pytest
 
 from vllm import LLM, PoolingParams
 from vllm.distributed import cleanup_dist_env_and_memory
+from vllm.exceptions import VLLMValidationError
 
 MODEL_NAME = "intfloat/multilingual-e5-small"
 
@@ -61,7 +62,7 @@ def test_multiple_pooling_params(llm: LLM):
     assert len(PROMPTS) == len(outputs)
 
     # Exception raised, if the size of params does not match the size of prompts
-    with pytest.raises(ValueError):
+    with pytest.raises(VLLMValidationError):
         outputs = llm.encode(
             PROMPTS, pooling_params=pooling_params[:3], pooling_task="embed"
         )
diff --git a/tests/entrypoints/pooling/test_io_processor.py b/tests/entrypoints/pooling/test_io_processor.py
new file mode 100644
index 0000000000..6c64966e58
--- /dev/null
+++ b/tests/entrypoints/pooling/test_io_processor.py
@@ -0,0 +1,76 @@
+# SPDX-License-Identifier: Apache-2.0
+# SPDX-FileCopyrightText: Copyright contributors to the vLLM project
+
+from types import SimpleNamespace
+
+import pytest
+
+from vllm import PoolingParams
+from vllm.entrypoints.pooling.base.io_processor import PoolingIOProcessor
+from vllm.entrypoints.pooling.typing import OfflineEncodeInputsContext
+from vllm.exceptions import VLLMValidationError
+from vllm.renderers import TokenizeParams
+
+
+@pytest.fixture
+def processor() -> PoolingIOProcessor:
+    return object.__new__(PoolingIOProcessor)
+
+
+def test_rejects_untrusted_request_chat_template(processor: PoolingIOProcessor):
+    with pytest.raises(VLLMValidationError) as exc_info:
+        processor._validate_chat_template("template", None, False)
+
+    assert str(exc_info.value) == (
+        "Chat template is passed with request, but "
+        "--trust-request-chat-template is not set. "
+        "Refused request with untrusted chat template."
+    )
+    assert exc_info.value.parameter is None
+    assert exc_info.value.value is None
+
+
+def test_rejects_mismatched_pooling_params(processor: PoolingIOProcessor):
+    with pytest.raises(VLLMValidationError) as exc_info:
+        processor._params_to_seq([PoolingParams()], num_requests=2)
+
+    assert str(exc_info.value) == (
+        "The lengths of prompts (2) and params (1) must be the same."
+    )
+    assert exc_info.value.parameter is None
+    assert exc_info.value.value is None
+
+
+def test_rejects_mismatched_lora_requests(processor: PoolingIOProcessor):
+    with pytest.raises(VLLMValidationError) as exc_info:
+        processor._lora_request_to_seq([None], num_requests=2)
+
+    assert str(exc_info.value) == (
+        "The lengths of prompts (2) and lora_request (1) must be the same."
+    )
+    assert exc_info.value.parameter is None
+    assert exc_info.value.value is None
+
+
+def test_rejects_conflicting_pooling_task(processor: PoolingIOProcessor):
+    processor.model_config = SimpleNamespace(is_encoder_decoder=False)
+    processor.renderer = SimpleNamespace(
+        default_cmpl_tok_params=TokenizeParams(max_total_tokens=None)
+    )
+    ctx = OfflineEncodeInputsContext(
+        pooling_task="embed",
+        tokenization_kwargs=None,
+        lora_request=None,
+        priorities=None,
+        prompts=[[1]],
+        pooling_params=PoolingParams(task="classify"),
+    )
+
+    with pytest.raises(VLLMValidationError) as exc_info:
+        processor.get_request_factory_offline(ctx)
+
+    assert str(exc_info.value) == (
+        "You cannot overwrite param.task='classify' with pooling_task='embed'!"
+    )
+    assert exc_info.value.parameter is None
+    assert exc_info.value.value is None
diff --git a/vllm/entrypoints/pooling/base/io_processor.py b/vllm/entrypoints/pooling/base/io_processor.py
index f74b740276..940987fc16 100644
--- a/vllm/entrypoints/pooling/base/io_processor.py
+++ b/vllm/entrypoints/pooling/base/io_processor.py
@@ -13,6 +13,7 @@ from vllm.config import VllmConfig
 from vllm.entrypoints.chat_utils import (
     ChatTemplateConfig,
 )
+from vllm.exceptions import VLLMValidationError
 from vllm.lora.request import LoRARequest
 from vllm.renderers import BaseRenderer, merge_kwargs
 from vllm.renderers.inputs.preprocess import parse_model_prompt, prompt_to_seq
@@ -217,7 +218,7 @@ class PoolingIOProcessor:
                 pass
             elif param.task != pooling_task:
                 msg = f"You cannot overwrite {param.task=!r} with {pooling_task=!r}!"
-                raise ValueError(msg)
+                raise VLLMValidationError(msg)
 
         seq_lora_requests = self._lora_request_to_seq(ctx.lora_request, num_requests)
         seq_priority = self._priority_to_seq(ctx.priorities, num_requests)
@@ -293,7 +294,7 @@ class PoolingIOProcessor:
                 and chat_template_kwargs.get("chat_template") is not None
             )
         ):
-            raise ValueError(
+            raise VLLMValidationError(
                 "Chat template is passed with request, but "
                 "--trust-request-chat-template is not set. "
                 "Refused request with untrusted chat template."
@@ -307,7 +308,7 @@ class PoolingIOProcessor:
     ) -> Sequence[PoolingParams]:
         if isinstance(params, Sequence):
             if len(params) != num_requests:
-                raise ValueError(
+                raise VLLMValidationError(
                     f"The lengths of prompts ({num_requests}) "
                     f"and params ({len(params)}) must be the same."
                 )
@@ -323,7 +324,7 @@ class PoolingIOProcessor:
     ) -> Sequence[LoRARequest | None]:
         if isinstance(lora_request, Sequence):
             if len(lora_request) != num_requests:
-                raise ValueError(
+                raise VLLMValidationError(
                     f"The lengths of prompts ({num_requests}) "
                     f"and lora_request ({len(lora_request)}) must be the same."
                 )