diff --git a/sdk/src/main/java/software/amazon/lambda/durable/DurableHandler.java b/sdk/src/main/java/software/amazon/lambda/durable/DurableHandler.java
index 966960979..3efdb24e3 100644
--- a/sdk/src/main/java/software/amazon/lambda/durable/DurableHandler.java
+++ b/sdk/src/main/java/software/amazon/lambda/durable/DurableHandler.java
@@ -130,6 +130,11 @@ public final void handleRequest(InputStream inputStream, OutputStream outputStre
         var inputString = new String(inputStream.readAllBytes());
         logger.debug("Raw input from durable handler: {}", inputString);
         var input = serDes.deserialize(inputString, TypeToken.get(DurableExecutionInput.class));
+        // Durable function inputs must contain DurableExecutionArn and CheckpointToken
+        if (input.durableExecutionArn() == null || input.checkpointToken() == null) {
+            throw new IllegalStateException(
+                    "Unexpected payload provided to start the durable execution. DurableConfig must be set in Lambda function configuration.");
+        }
         var output = DurableExecutor.execute(input, context, inputType, this::handleRequest, config);
         outputStream.write(serDes.serialize(output).getBytes());
     }
diff --git a/sdk/src/test/java/software/amazon/lambda/durable/DurableHandlerTest.java b/sdk/src/test/java/software/amazon/lambda/durable/DurableHandlerTest.java
index 922c048d7..f823ec1dc 100644
--- a/sdk/src/test/java/software/amazon/lambda/durable/DurableHandlerTest.java
+++ b/sdk/src/test/java/software/amazon/lambda/durable/DurableHandlerTest.java
@@ -4,7 +4,12 @@
 
 import static org.junit.jupiter.api.Assertions.assertEquals;
 import static org.junit.jupiter.api.Assertions.assertNotNull;
+import static org.junit.jupiter.api.Assertions.assertThrows;
+import static org.junit.jupiter.api.Assertions.assertTrue;
 
+import java.io.ByteArrayInputStream;
+import java.io.ByteArrayOutputStream;
+import java.nio.charset.StandardCharsets;
 import org.junit.jupiter.api.Test;
 
 class DurableHandlerTest {
@@ -47,6 +52,19 @@ public Object handleRequest(Object input, DurableContext context) {
         }
     }
 
+    @Test
+    void testNonDurableFunctionThrowsUserFriendlyError() throws Exception {
+        var handler = new TestDurableHandler();
+        // Durable function inputs must contain DurableExecutionArn and CheckpointToken
+        var nonDurableInput = "{\"input\": \"non-durable\"}";
+        var inputStream = new ByteArrayInputStream(nonDurableInput.getBytes(StandardCharsets.UTF_8));
+        var outputStream = new ByteArrayOutputStream();
+
+        var exception =
+                assertThrows(IllegalStateException.class, () -> handler.handleRequest(inputStream, outputStream, null));
+        assertTrue(exception.getMessage().contains("Unexpected payload provided to start the durable execution"));
+    }
+
     // Test handler implementation
     private static class TestDurableHandler extends DurableHandler<String, String> {
         @Override