diff --git a/components/src/dynamo/frontend/tests/test_vllm_processor_unit.py b/components/src/dynamo/frontend/tests/test_vllm_processor_unit.py
index 0989298a8f92..cc60165b34c1 100644
--- a/components/src/dynamo/frontend/tests/test_vllm_processor_unit.py
+++ b/components/src/dynamo/frontend/tests/test_vllm_processor_unit.py
@@ -1859,6 +1859,17 @@ async def generate(self, preprocessed, **kwargs):
         # The serialized envelope must not leak to the client.
         assert "BackendInvalidArgument" not in excinfo.value.message
 
+    @pytest.mark.asyncio
+    async def test_invalid_argument_rejection_propagates(self, vllm_processor_module):
+        class _RefusingEngine(_FakeRoutedEngine):
+            async def generate(self, preprocessed, **kwargs):
+                raise InvalidArgument("use --enable-multimodal")
+
+        processor = _make_processor(vllm_processor_module, _RefusingEngine())
+
+        with pytest.raises(InvalidArgument, match="--enable-multimodal"):
+            await _run_generate(processor, _base_preproc())
+
     @pytest.mark.asyncio
     async def test_genuine_internal_failure_is_still_internal(
         self, vllm_processor_module
diff --git a/components/src/dynamo/frontend/vllm_processor.py b/components/src/dynamo/frontend/vllm_processor.py
index 64514d486d1f..81be99844b74 100644
--- a/components/src/dynamo/frontend/vllm_processor.py
+++ b/components/src/dynamo/frontend/vllm_processor.py
@@ -41,7 +41,7 @@
 from dynamo.common.utils.input_params import resolve_thinking_token_budget
 from dynamo.frontend.frontend_args import FrontendConfig
 from dynamo.llm import ModelCardInstanceId, PythonAsyncEngine, RoutedEngine
-from dynamo.llm.exceptions import HttpError
+from dynamo.llm.exceptions import HttpError, InvalidArgument
 from dynamo.vllm.errors import vllm_client_error_to_http_error
 
 from .prepost import StreamingPostProcessor, preprocess_chat_request
@@ -1415,6 +1415,8 @@ async def _generate_and_stream(
             # translates them at Dynamo's HTTP boundary. The generic handler
             # below is reserved for genuine internal failures.
             raise
+        except InvalidArgument:
+            raise
         except Exception as e:
             backend_error = backend_invalid_argument_to_http_error(e)
             if backend_error is not None:
diff --git a/components/src/dynamo/vllm/handlers.py b/components/src/dynamo/vllm/handlers.py
index 99e0ecd2e383..6dc7cba89ed7 100644
--- a/components/src/dynamo/vllm/handlers.py
+++ b/components/src/dynamo/vllm/handlers.py
@@ -3817,12 +3817,11 @@ async def _assemble_custom_encoder_prompt(
             # Log with the traceback here — this is the last frame that knows
             # which request and which encoder — then re-raise unchanged.
             #
-            # Deliberately not converted to `InvalidArgument`. The adapters
-            # raise `ValueError`/`TypeError` for genuine input faults, which the
-            # bindings already map to `Backend(InvalidArgument)` → 400 carrying
-            # the message, so the actionable case needs no help. Coercing the
-            # rest would relabel timeouts, CUDA faults, batcher shutdown and
-            # cancellations as client errors, suppressing retries — and since
+            # Deliberately not converted to `InvalidArgument`: adapter
+            # `ValueError`/`TypeError` map to 400, but with a generic
+            # body — only `InvalidArgument` carries its message to the client.
+            # Coercing the rest would relabel timeouts, CUDA faults, batcher shutdown
+            # and cancellations as client errors, suppressing retries — and since
             # `encode()` is co-batched, it could blame a caller for a failure
             # that originated in someone else's request.
             logger.exception("Request %s: CustomEncoder failed", request_id)
diff --git a/lib/bindings/python/rust/errors.rs b/lib/bindings/python/rust/errors.rs
index 9fe735d0e7b6..763159167f79 100644
--- a/lib/bindings/python/rust/errors.rs
+++ b/lib/bindings/python/rust/errors.rs
@@ -161,6 +161,24 @@ fn public_invalid_request_message(error: &DynamoError) -> Option<&str> {
     }
 }
 
+fn public_invalid_argument_message(err: &(dyn std::error::Error + 'static)) -> Option<String> {
+    let mut current = Some(err);
+    while let Some(error) = current {
+        if let Some(dynamo_err) = error.downcast_ref::<DynamoError>() {
+            return public_invalid_request_message(dynamo_err).map(str::to_owned);
+        }
+        current = error.source();
+    }
+    None
+}
+
+pub fn semantic_to_pyerr(err: &anyhow::Error) -> PyErr {
+    if let Some(message) = public_invalid_argument_message(err.as_ref()) {
+        return InvalidArgument::new_err(message);
+    }
+    pyo3::exceptions::PyException::new_err(format!("{err}"))
+}
+
 /// Read `(code, message)` off a Python exception carrying an HTTP-style
 /// status. Accepts `.code` (matches [`HttpError`] in `http.rs`) or `.status`
 /// (matches `dynamo.common.http.HttpStatusError`) plus `.message`.
@@ -264,6 +282,35 @@ mod tests {
         assert_eq!(public_invalid_request_message(&error), None);
     }
 
+    #[derive(Debug)]
+    struct RouterWrapped(DynamoError);
+
+    impl std::fmt::Display for RouterWrapped {
+        fn fmt(&self, f: &mut std::fmt::Formatter<'_>) -> std::fmt::Result {
+            write!(f, "Prefill execution failed: {}", self.0)
+        }
+    }
+
+    impl std::error::Error for RouterWrapped {
+        fn source(&self) -> Option<&(dyn std::error::Error + 'static)> {
+            Some(&self.0)
+        }
+    }
+
+    #[test]
+    fn error_chain_yields_public_invalid_argument_message() {
+        let worker_error = DynamoError::builder()
+            .class(ErrorClass::InvalidRequest)
+            .diagnostic("private backend detail")
+            .public_message("use --enable-multimodal")
+            .build();
+        let wrapped = anyhow::Error::new(RouterWrapped(worker_error));
+        assert_eq!(
+            public_invalid_argument_message(wrapped.as_ref()),
+            Some("use --enable-multimodal".to_string())
+        );
+    }
+
     #[test]
     fn other_error_classes_are_not_promoted_to_invalid_arguments() {
         for class in [
diff --git a/lib/bindings/python/rust/llm/routed_engine.rs b/lib/bindings/python/rust/llm/routed_engine.rs
index 47e228792ece..635a6700d6d3 100644
--- a/lib/bindings/python/rust/llm/routed_engine.rs
+++ b/lib/bindings/python/rust/llm/routed_engine.rs
@@ -68,7 +68,10 @@ impl RoutedEngine {
         crate::future_into_py(
             py,
             async move {
-                let mut stream = inner.generate(request_context).await.map_err(to_pyerr)?;
+                let mut stream = inner
+                    .generate(request_context)
+                    .await
+                    .map_err(|e| crate::errors::semantic_to_pyerr(&e))?;
                 let task_context = stream.context();
                 let (tx, rx) = tokio::sync::mpsc::channel::<RsAnnotated<PyObject>>(32);
 
diff --git a/lib/llm/src/kv_router/prefill_router/mod.rs b/lib/llm/src/kv_router/prefill_router/mod.rs
index 2569cd7edb93..5cffa80f3afe 100644
--- a/lib/llm/src/kv_router/prefill_router/mod.rs
+++ b/lib/llm/src/kv_router/prefill_router/mod.rs
@@ -78,9 +78,10 @@ pub enum PrefillError {
     #[error("Prefill router not yet activated")]
     NotActivated,
 
-    // Callers must include the worker's error text in this message. The
-    // frontend receives this error through `to_pyerr`, which keeps only
-    // `Display` and drops the source chain, so a `#[source]` is never seen.
+    // Callers must include the worker's error text in this message.
+    // The frontend boundary walks the `#[source]` chain, so a classified
+    // InvalidRequest with a public message reaches the client with its own
+    // text.
     #[error("Prefill execution failed: {0}")]
     PrefillError(
         String,