diff --git a/sdks/java/io/rrio/src/main/java/org/apache/beam/io/requestresponse/Call.java b/sdks/java/io/rrio/src/main/java/org/apache/beam/io/requestresponse/Call.java
index ab73946534cd..112d1dd9229b 100644
--- a/sdks/java/io/rrio/src/main/java/org/apache/beam/io/requestresponse/Call.java
+++ b/sdks/java/io/rrio/src/main/java/org/apache/beam/io/requestresponse/Call.java
@@ -46,6 +46,7 @@
 import org.apache.beam.sdk.values.PCollectionTuple;
 import org.apache.beam.sdk.values.TupleTag;
 import org.apache.beam.sdk.values.TupleTagList;
+import org.apache.beam.vendor.guava.v32_1_2_jre.com.google.common.base.Throwables;
 import org.checkerframework.checker.nullness.qual.MonotonicNonNull;
 import org.joda.time.Duration;
 
@@ -613,12 +614,32 @@ private void executeAsync(Callable<Void> callable) throws UserCodeExecutionExcep
   private static <T> void parseAndThrow(Future<T> future, ExecutionException e)
       throws UserCodeExecutionException {
     future.cancel(true);
-    if (e.getCause() == null) {
-      throw new UserCodeExecutionException(e);
+
+    try {
+      UserCodeExecutionException genericException = null;
+      for (Throwable throwable : Throwables.getCausalChain(e)) {
+        if (throwable instanceof UserCodeQuotaException) {
+          throw (UserCodeQuotaException) throwable;
+        } else if (throwable instanceof UserCodeTimeoutException) {
+          throw (UserCodeTimeoutException) throwable;
+        } else if (throwable instanceof UserCodeRemoteSystemException) {
+          throw (UserCodeRemoteSystemException) throwable;
+        } else if (genericException == null && throwable instanceof UserCodeExecutionException) {
+          genericException = (UserCodeExecutionException) throwable;
+        }
+      }
+      if (genericException != null) {
+        throw genericException;
+      }
+    } catch (IllegalArgumentException iae) {
+      // Circular reference detected in causal chain
+      throw new UserCodeExecutionException(
+          "circular reference detected in exception causal chain", e);
     }
-    Throwable cause = checkStateNotNull(e.getCause());
-    if (cause instanceof UserCodeQuotaException) {
-      throw new UserCodeQuotaException(cause);
+
+    Throwable cause = e.getCause();
+    if (cause == null) {
+      throw new UserCodeExecutionException(e);
     }
     throw new UserCodeExecutionException(cause);
   }
diff --git a/sdks/java/io/rrio/src/test/java/org/apache/beam/io/requestresponse/CallTest.java b/sdks/java/io/rrio/src/test/java/org/apache/beam/io/requestresponse/CallTest.java
index 0e572bdd2d64..4784f40f1822 100644
--- a/sdks/java/io/rrio/src/test/java/org/apache/beam/io/requestresponse/CallTest.java
+++ b/sdks/java/io/rrio/src/test/java/org/apache/beam/io/requestresponse/CallTest.java
@@ -104,6 +104,34 @@ public void givenCallerThrowsUserCodeExecutionException_emitsIntoFailurePCollect
     pipeline.run();
   }
 
+  @Test
+  public void givenCallerThrowsNonUserCodeException_emitsWrappedUserCodeExecutionException() {
+    Result<Response> result =
+        pipeline
+            .apply(Create.of(new Request("a")))
+            .apply(Call.of(new CallerThrowsRuntimeException(), NON_DETERMINISTIC_RESPONSE_CODER));
+
+    PCollection<ApiIOError> failures = result.getFailures();
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeExecutionException.class))
+        .isEqualTo(1L);
+
+    pipeline.run();
+  }
+
+  @Test
+  public void givenCallerThrowsCircularCausalChain_emitsUserCodeExecutionException() {
+    Result<Response> result =
+        pipeline
+            .apply(Create.of(new Request("a")))
+            .apply(Call.of(new CallerThrowsCircularCause(), NON_DETERMINISTIC_RESPONSE_CODER));
+
+    PCollection<ApiIOError> failures = result.getFailures();
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeExecutionException.class))
+        .isEqualTo(1L);
+
+    pipeline.run();
+  }
+
   @Test
   public void givenCallerThrowsQuotaException_emitsIntoFailurePCollection() {
     Result<Response> result =
@@ -142,7 +170,7 @@ public void givenCallerTimeout_emitsFailurePCollection() {
   }
 
   @Test
-  public void givenCallerThrowsTimeoutException_emitsFailurePCollection() {
+  public void givenCallerThrowsTimeoutException_thenPreservesExceptionType() {
     Result<Response> result =
         pipeline
             .apply(Create.of(new Request("a")))
@@ -150,7 +178,7 @@ public void givenCallerThrowsTimeoutException_emitsFailurePCollection() {
 
     PCollection<ApiIOError> failures = result.getFailures();
     PAssert.thatSingleton(countStackTracesOf(failures, UserCodeExecutionException.class))
-        .isEqualTo(1L);
+        .isEqualTo(0L);
     PAssert.thatSingleton(countStackTracesOf(failures, UserCodeQuotaException.class)).isEqualTo(0L);
     PAssert.thatSingleton(countStackTracesOf(failures, UserCodeTimeoutException.class))
         .isEqualTo(1L);
@@ -158,6 +186,153 @@ public void givenCallerThrowsTimeoutException_emitsFailurePCollection() {
     pipeline.run();
   }
 
+  @Test
+  public void givenCallerThrowsRemoteSystemException_thenPreservesExceptionType() {
+    Result<Response> result =
+        pipeline
+            .apply(Create.of(new Request("a")))
+            .apply(
+                Call.of(new CallerThrowsRemoteSystemException(), NON_DETERMINISTIC_RESPONSE_CODER));
+
+    PCollection<ApiIOError> failures = result.getFailures();
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeRemoteSystemException.class))
+        .isEqualTo(1L);
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeExecutionException.class))
+        .isEqualTo(0L);
+
+    pipeline.run();
+  }
+
+  @Test
+  public void givenNestedExecutionException_thenPreservesExceptionType() {
+    Result<Response> result =
+        pipeline
+            .apply(Create.of(new Request("a")))
+            .apply(
+                Call.of(
+                    new CallerThrowsNestedExecutionException(), NON_DETERMINISTIC_RESPONSE_CODER));
+
+    PCollection<ApiIOError> failures = result.getFailures();
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeExecutionException.class))
+        .isEqualTo(1L);
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeTimeoutException.class))
+        .isEqualTo(0L);
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeRemoteSystemException.class))
+        .isEqualTo(0L);
+
+    pipeline.run();
+  }
+
+  @Test
+  public void givenCallerThrowsGenericWrappingTimeout_thenPreservesExceptionType() {
+    Result<Response> result =
+        pipeline
+            .apply(Create.of(new Request("a")))
+            .apply(
+                Call.of(
+                    new CallerThrowsGenericWrappingTimeout(), NON_DETERMINISTIC_RESPONSE_CODER));
+
+    PCollection<ApiIOError> failures = result.getFailures();
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeTimeoutException.class))
+        .isEqualTo(1L);
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeExecutionException.class))
+        .isEqualTo(0L);
+
+    pipeline.run();
+  }
+
+  @Test
+  public void givenCallerThrowsGenericWrappingQuota_thenPreservesExceptionType() {
+    Result<Response> result =
+        pipeline
+            .apply(Create.of(new Request("a")))
+            .apply(
+                Call.of(new CallerThrowsGenericWrappingQuota(), NON_DETERMINISTIC_RESPONSE_CODER));
+
+    PCollection<ApiIOError> failures = result.getFailures();
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeQuotaException.class)).isEqualTo(1L);
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeExecutionException.class))
+        .isEqualTo(0L);
+
+    pipeline.run();
+  }
+
+  @Test
+  public void givenCallerThrowsGenericWrappingRemoteSystem_thenPreservesExceptionType() {
+    Result<Response> result =
+        pipeline
+            .apply(Create.of(new Request("a")))
+            .apply(
+                Call.of(
+                    new CallerThrowsGenericWrappingRemoteSystem(),
+                    NON_DETERMINISTIC_RESPONSE_CODER));
+
+    PCollection<ApiIOError> failures = result.getFailures();
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeRemoteSystemException.class))
+        .isEqualTo(1L);
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeExecutionException.class))
+        .isEqualTo(0L);
+
+    pipeline.run();
+  }
+
+  @Test
+  public void
+      givenCallerThrowsUncheckedExecutionExceptionWrappingTimeout_thenPreservesExceptionType() {
+    Result<Response> result =
+        pipeline
+            .apply(Create.of(new Request("a")))
+            .apply(
+                Call.of(
+                    new CallerThrowsUncheckedExecutionExceptionWrappingTimeout(),
+                    NON_DETERMINISTIC_RESPONSE_CODER));
+
+    PCollection<ApiIOError> failures = result.getFailures();
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeTimeoutException.class))
+        .isEqualTo(1L);
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeExecutionException.class))
+        .isEqualTo(0L);
+
+    pipeline.run();
+  }
+
+  @Test
+  public void
+      givenCallerThrowsUncheckedExecutionExceptionWrappingRemoteSystem_thenPreservesExceptionType() {
+    Result<Response> result =
+        pipeline
+            .apply(Create.of(new Request("a")))
+            .apply(
+                Call.of(
+                    new CallerThrowsUncheckedExecutionExceptionWrappingRemoteSystem(),
+                    NON_DETERMINISTIC_RESPONSE_CODER));
+
+    PCollection<ApiIOError> failures = result.getFailures();
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeRemoteSystemException.class))
+        .isEqualTo(1L);
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeExecutionException.class))
+        .isEqualTo(0L);
+
+    pipeline.run();
+  }
+
+  @Test
+  public void givenCallerThrowsTripleNestedTimeout_thenPreservesExceptionType() {
+    Result<Response> result =
+        pipeline
+            .apply(Create.of(new Request("a")))
+            .apply(
+                Call.of(new CallerThrowsTripleNestedTimeout(), NON_DETERMINISTIC_RESPONSE_CODER));
+
+    PCollection<ApiIOError> failures = result.getFailures();
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeTimeoutException.class))
+        .isEqualTo(1L);
+    PAssert.thatSingleton(countStackTracesOf(failures, UserCodeExecutionException.class))
+        .isEqualTo(0L);
+
+    pipeline.run();
+  }
+
   @Test
   public void givenSetupThrowsUserCodeExecutionException_throwsError() {
     pipeline
@@ -376,6 +551,25 @@ public Response call(Request request) throws UserCodeExecutionException {
     }
   }
 
+  private static class CallerThrowsRuntimeException implements Caller<Request, Response> {
+
+    @Override
+    public Response call(Request request) {
+      throw new RuntimeException("unexpected error");
+    }
+  }
+
+  private static class CallerThrowsCircularCause implements Caller<Request, Response> {
+
+    @Override
+    public Response call(Request request) {
+      Exception a = new Exception("a");
+      Exception b = new Exception("b", a);
+      a.initCause(b); // a -> b -> a (circular reference)
+      throw new RuntimeException("boom", a);
+    }
+  }
+
   private static class CallerThrowsTimeout implements Caller<Request, Response> {
 
     @Override
@@ -384,6 +578,74 @@ public Response call(Request request) throws UserCodeExecutionException {
     }
   }
 
+  private static class CallerThrowsRemoteSystemException implements Caller<Request, Response> {
+
+    @Override
+    public Response call(Request request) throws UserCodeExecutionException {
+      throw new UserCodeRemoteSystemException("");
+    }
+  }
+
+  private static class CallerThrowsNestedExecutionException implements Caller<Request, Response> {
+
+    @Override
+    public Response call(Request request) throws UserCodeExecutionException {
+      throw new UncheckedExecutionException(new UserCodeExecutionException("nested"));
+    }
+  }
+
+  private static class CallerThrowsGenericWrappingTimeout implements Caller<Request, Response> {
+
+    @Override
+    public Response call(Request request) throws UserCodeExecutionException {
+      throw new UserCodeExecutionException("generic", new UserCodeTimeoutException("timeout"));
+    }
+  }
+
+  private static class CallerThrowsGenericWrappingQuota implements Caller<Request, Response> {
+
+    @Override
+    public Response call(Request request) throws UserCodeExecutionException {
+      throw new UserCodeExecutionException("generic", new UserCodeQuotaException("quota"));
+    }
+  }
+
+  private static class CallerThrowsGenericWrappingRemoteSystem
+      implements Caller<Request, Response> {
+
+    @Override
+    public Response call(Request request) throws UserCodeExecutionException {
+      throw new UserCodeExecutionException("generic", new UserCodeRemoteSystemException("remote"));
+    }
+  }
+
+  private static class CallerThrowsUncheckedExecutionExceptionWrappingTimeout
+      implements Caller<Request, Response> {
+
+    @Override
+    public Response call(Request request) throws UserCodeExecutionException {
+      throw new UncheckedExecutionException(new UserCodeTimeoutException("timeout"));
+    }
+  }
+
+  private static class CallerThrowsUncheckedExecutionExceptionWrappingRemoteSystem
+      implements Caller<Request, Response> {
+
+    @Override
+    public Response call(Request request) throws UserCodeExecutionException {
+      throw new UncheckedExecutionException(new UserCodeRemoteSystemException("remote"));
+    }
+  }
+
+  private static class CallerThrowsTripleNestedTimeout implements Caller<Request, Response> {
+
+    @Override
+    public Response call(Request request) throws UserCodeExecutionException {
+      throw new UncheckedExecutionException(
+          new RuntimeException(new UserCodeTimeoutException("deep timeout")));
+    }
+  }
+
   private static class CallerInvokesQuotaException implements Caller<Request, Response> {
 
     @Override
diff --git a/sdks/python/apache_beam/transforms/ptransform.py b/sdks/python/apache_beam/transforms/ptransform.py
index 9c5306e143ec..94e9a0644d04 100644
--- a/sdks/python/apache_beam/transforms/ptransform.py
+++ b/sdks/python/apache_beam/transforms/ptransform.py
@@ -883,8 +883,15 @@ def __init__(self, fn, *args, **kwargs):
     # Ensure fn and side inputs are picklable for remote execution.
     try:
       self.fn = pickler.roundtrip(self.fn)
-    except RuntimeError as e:
-      raise RuntimeError('Unable to pickle fn %s: %s' % (self.fn, e))
+    except (RuntimeError, TypeError, Exception) as e:
+      raise RuntimeError(
+          'Unable to pickle fn %s: %s. '
+          'User code must be serializable (picklable) for distributed '
+          'execution. This usually happens when lambdas or closures capture '
+          'non-serializable objects like file handles, database connections, '
+          'or thread locks. Try: (1) using module-level functions instead of '
+          'lambdas, (2) initializing resources in setup() methods, '
+          '(3) checking what your closure captures.' % (self.fn, e)) from e
 
     self.args = pickler.roundtrip(self.args)
     self.kwargs = pickler.roundtrip(self.kwargs)
diff --git a/sdks/python/apache_beam/transforms/ptransform_test.py b/sdks/python/apache_beam/transforms/ptransform_test.py
index 9a9bf6ff0a74..8c2acefccdb3 100644
--- a/sdks/python/apache_beam/transforms/ptransform_test.py
+++ b/sdks/python/apache_beam/transforms/ptransform_test.py
@@ -163,6 +163,25 @@ def test_do_with_side_input_as_keyword_arg(self):
           lambda x, addon: [x + addon], addon=pvalue.AsSingleton(side))
       assert_that(result, equal_to([11, 12, 13]))
 
+  def test_callable_non_serializable_error_message(self):
+    class NonSerializable:
+      def __getstate__(self):
+        raise RuntimeError('nope')
+
+    bad = NonSerializable()
+
+    with self.assertRaises(RuntimeError) as context:
+      _ = beam.Map(lambda x: bad)
+
+    message = str(context.exception)
+    self.assertIn('Unable to pickle fn', message)
+    self.assertIn(
+        'User code must be serializable (picklable) for distributed execution.',
+        message)
+    self.assertIn('non-serializable objects like file handles', message)
+    self.assertIn(
+        'Try: (1) using module-level functions instead of lambdas', message)
+
   def test_do_with_do_fn_returning_string_raises_warning(self):
     ex_details = r'.*Returning a str from a ParDo or FlatMap is discouraged.'