diff --git a/packages/react-native/src/private/renderer/core/__tests__/EventTargetDispatching-itest.js b/packages/react-native/src/private/renderer/core/__tests__/EventTargetDispatching-itest.js
index 76de52d98711..8336899f4c5f 100644
--- a/packages/react-native/src/private/renderer/core/__tests__/EventTargetDispatching-itest.js
+++ b/packages/react-native/src/private/renderer/core/__tests__/EventTargetDispatching-itest.js
@@ -1327,15 +1327,7 @@ const {isOSS} = Fantom.getConstants();
       expect(order).toEqual(['parent-capture']);
     });
 
-    // When enableNativeEventTargetEventDispatching is true, EventTarget.js
-    // defers handler errors via setTimeout(0) in reportListenerError. This
-    // leaves a pending callback that Fantom's validateEmptyMessageQueue
-    // catches, and the error leaks into subsequent tests. Skip in that
-    // configuration until the error propagation mechanism is made
-    // synchronous (matching the legacy rethrowCaughtError pattern).
-    (ReactNativeFeatureFlags.enableNativeEventTargetEventDispatching()
-      ? describe.skip
-      : describe)('error handling', () => {
+    describe('error handling', () => {
       it('error in event handler does not break dispatch to subsequent listeners', () => {
         const root = Fantom.createRoot();
         const childRef = React.createRef<React.ElementRef<typeof View>>();
diff --git a/packages/react-native/src/private/renderer/events/dispatchNativeEvent.js b/packages/react-native/src/private/renderer/events/dispatchNativeEvent.js
index 1013ad98687f..69efbb30fea4 100644
--- a/packages/react-native/src/private/renderer/events/dispatchNativeEvent.js
+++ b/packages/react-native/src/private/renderer/events/dispatchNativeEvent.js
@@ -44,64 +44,75 @@ export default function dispatchNativeEvent(
   // Process responder events before normal event dispatch.
   processResponderEvent(type, target, payload);
 
-  // Normal EventTarget dispatch
-  const bubbleConfig = customBubblingEventTypes[type];
-  const directConfig = customDirectEventTypes[type];
+  try {
+    // Normal EventTarget dispatch
+    const bubbleConfig = customBubblingEventTypes[type];
+    const directConfig = customDirectEventTypes[type];
 
-  // Skip events that are not registered in the view config
-  if (bubbleConfig != null || directConfig != null) {
-    // Honor `skipBubbling` declared in the view config: when set, the bubble
-    // phase only fires on the target itself (matching the legacy renderer's
-    // behavior). The synthesized event reports `bubbles: false`, which causes
-    // the EventTarget bubble loop to short-circuit after dispatching to the
-    // target. Capture-phase listeners are unaffected.
-    const bubbles =
-      bubbleConfig != null &&
-      bubbleConfig.phasedRegistrationNames.skipBubbling !== true;
+    // Skip events that are not registered in the view config
+    if (bubbleConfig != null || directConfig != null) {
+      // Honor `skipBubbling` declared in the view config: when set, the bubble
+      // phase only fires on the target itself (matching the legacy renderer's
+      // behavior). The synthesized event reports `bubbles: false`, which causes
+      // the EventTarget bubble loop to short-circuit after dispatching to the
+      // target. Capture-phase listeners are unaffected.
+      const bubbles =
+        bubbleConfig != null &&
+        bubbleConfig.phasedRegistrationNames.skipBubbling !== true;
 
-    const eventType = topLevelTypeToEventType(type);
-    const options: {bubbles: boolean, cancelable: boolean} = {
-      bubbles,
-      cancelable: true,
-    };
+      const eventType = topLevelTypeToEventType(type);
+      const options: {bubbles: boolean, cancelable: boolean} = {
+        bubbles,
+        cancelable: true,
+      };
 
-    // Preserve the native event timestamp for backwards compatibility.
-    const nativeTimestamp = payload.timeStamp ?? payload.timestamp;
-    if (typeof nativeTimestamp === 'number') {
-      setEventInitTimeStamp(options, nativeTimestamp);
-    }
-
-    const syntheticEvent = new LegacySyntheticEvent(
-      eventType,
-      options,
-      payload,
-      bubbleConfig ?? directConfig,
-    );
+      // Preserve the native event timestamp for backwards compatibility.
+      const nativeTimestamp = payload.timeStamp ?? payload.timestamp;
+      if (typeof nativeTimestamp === 'number') {
+        setEventInitTimeStamp(options, nativeTimestamp);
+      }
 
-    // Pre-resolve the React prop names ("onFoo" / "onFooCapture") once per
-    // dispatch and stash them on the event so per-ancestor
-    // `EVENT_TARGET_GET_DECLARATIVE_LISTENER_KEY` lookups can read them
-    // directly, avoiding the per-call `getEventTypePropName` hash lookup.
-    if (bubbleConfig != null) {
-      const phasedRegistrationNames = bubbleConfig.phasedRegistrationNames;
-      setBubbledPropName(
-        syntheticEvent,
-        phasedRegistrationNames.bubbled ?? null,
+      const syntheticEvent = new LegacySyntheticEvent(
+        eventType,
+        options,
+        payload,
+        bubbleConfig ?? directConfig,
       );
-      setCapturedPropName(
-        syntheticEvent,
-        phasedRegistrationNames.captured ?? null,
-      );
-    } else if (directConfig != null) {
-      setBubbledPropName(syntheticEvent, directConfig.registrationName ?? null);
-      setCapturedPropName(syntheticEvent, null);
-    }
 
-    dispatchTrustedEvent(target, syntheticEvent);
-  }
+      // Pre-resolve the React prop names ("onFoo" / "onFooCapture") once per
+      // dispatch and stash them on the event so per-ancestor
+      // `EVENT_TARGET_GET_DECLARATIVE_LISTENER_KEY` lookups can read them
+      // directly, avoiding the per-call `getEventTypePropName` hash lookup.
+      if (bubbleConfig != null) {
+        const phasedRegistrationNames = bubbleConfig.phasedRegistrationNames;
+        setBubbledPropName(
+          syntheticEvent,
+          phasedRegistrationNames.bubbled ?? null,
+        );
+        setCapturedPropName(
+          syntheticEvent,
+          phasedRegistrationNames.captured ?? null,
+        );
+      } else if (directConfig != null) {
+        setBubbledPropName(
+          syntheticEvent,
+          directConfig.registrationName ?? null,
+        );
+        setCapturedPropName(syntheticEvent, null);
+      }
 
-  // Rethrow the first error caught during responder lifecycle dispatch,
-  // after all dispatching is complete. This matches the old system's
-  // runEventsInBatch → rethrowCaughtError pattern.
-  rethrowCaughtError();
+      // Pass `rethrowListenerErrors: true` so the first listener error is
+      // rethrown synchronously (matching the legacy plugin path) rather than
+      // deferred to a new task, keeping it catchable by React error boundaries
+      // and the native event call.
+      dispatchTrustedEvent(target, syntheticEvent, true);
+    }
+  } finally {
+    // Rethrow the first error caught during responder lifecycle dispatch,
+    // after all dispatching is complete. This matches the old system's
+    // runEventsInBatch → rethrowCaughtError pattern. Running it in a `finally`
+    // ensures a pending responder error is never left to leak into a later
+    // dispatch even if the normal dispatch above threw synchronously.
+    rethrowCaughtError();
+  }
 }
diff --git a/packages/react-native/src/private/webapis/dom/events/EventTarget.js b/packages/react-native/src/private/webapis/dom/events/EventTarget.js
index e794efcc3379..51a16621617c 100644
--- a/packages/react-native/src/private/webapis/dom/events/EventTarget.js
+++ b/packages/react-native/src/private/webapis/dom/events/EventTarget.js
@@ -207,7 +207,7 @@ export default class EventTarget {
 
     setIsTrusted(event, false);
 
-    dispatch(this, event);
+    dispatch(this, event, false);
 
     return !event.defaultPrevented;
   }
@@ -249,8 +249,11 @@ export default class EventTarget {
    * canceled (i.e. `event.defaultPrevented`), otherwise `true`.
    */
   // $FlowExpectedError[unsupported-syntax]
-  [INTERNAL_DISPATCH_METHOD_KEY](event: Event): boolean {
-    dispatch(this, event);
+  [INTERNAL_DISPATCH_METHOD_KEY](
+    event: Event,
+    rethrowListenerErrors?: boolean,
+  ): boolean {
+    dispatch(this, event, rethrowListenerErrors === true);
     return !event.defaultPrevented;
   }
 }
@@ -280,13 +283,26 @@ function getDefaultPassiveValue(
  * Implements the "event dispatch" concept
  * (see https://dom.spec.whatwg.org/#concept-event-dispatch).
  */
-function dispatch(eventTarget: EventTarget, event: Event): void {
+function dispatch(
+  eventTarget: EventTarget,
+  event: Event,
+  rethrowErrors: boolean,
+): void {
   setEventDispatchFlag(event, true);
 
   const eventPath = getEventPath(eventTarget, event);
   setComposedPath(event, eventPath);
   setTarget(event, eventTarget);
 
+  // When `rethrowErrors` is set (trusted dispatch of native UI events), collect
+  // the first listener error and rethrow it synchronously once the dispatch
+  // completes, matching the legacy plugin system's `rethrowCaughtError`
+  // behavior. Otherwise (the public `dispatchEvent` API, XHR, etc.) listener
+  // errors are reported to the global error handler per the DOM spec.
+  const errorState: ListenerErrorState | null = rethrowErrors
+    ? {hasError: false, error: undefined}
+    : null;
+
   for (let i = eventPath.length - 1; i >= 0; i--) {
     if (getStopPropagationFlag(event)) {
       break;
@@ -297,7 +313,7 @@ function dispatch(eventTarget: EventTarget, event: Event): void {
       event,
       target === eventTarget ? Event.AT_TARGET : Event.CAPTURING_PHASE,
     );
-    invoke(target, event, Event.CAPTURING_PHASE);
+    invoke(target, event, Event.CAPTURING_PHASE, errorState);
   }
 
   for (const target of eventPath) {
@@ -315,7 +331,7 @@ function dispatch(eventTarget: EventTarget, event: Event): void {
       event,
       target === eventTarget ? Event.AT_TARGET : Event.BUBBLING_PHASE,
     );
-    invoke(target, event, Event.BUBBLING_PHASE);
+    invoke(target, event, Event.BUBBLING_PHASE, errorState);
   }
 
   setEventPhase(event, Event.NONE);
@@ -325,6 +341,12 @@ function dispatch(eventTarget: EventTarget, event: Event): void {
   setEventDispatchFlag(event, false);
   setStopImmediatePropagationFlag(event, false);
   setStopPropagationFlag(event, false);
+
+  // Trusted dispatch: surface the first listener error synchronously, after the
+  // event has been fully cleaned up.
+  if (errorState != null && errorState.hasError) {
+    throw errorState.error;
+  }
 }
 
 /**
@@ -356,6 +378,7 @@ function invoke(
   eventTarget: EventTarget,
   event: Event,
   eventPhase: EventPhase,
+  errorState: ListenerErrorState | null,
 ) {
   const isCapture = eventPhase === Event.CAPTURING_PHASE;
 
@@ -385,7 +408,7 @@ function invoke(
       try {
         propListener.call(eventTarget, event);
       } catch (error) {
-        reportListenerError(error);
+        handleListenerError(error, errorState);
       }
       global.event = currentEvent;
       return;
@@ -404,7 +427,7 @@ function invoke(
     for (const registration of maybeListeners.values()) {
       listeners.push(registration);
     }
-    invokeListeners(eventTarget, event, listeners, isCapture);
+    invokeListeners(eventTarget, event, listeners, isCapture, errorState);
     return;
   }
 
@@ -419,6 +442,7 @@ function invoke(
     event,
     Array.from(maybeListeners.values()),
     isCapture,
+    errorState,
   );
 }
 
@@ -427,6 +451,7 @@ function invokeListeners(
   event: Event,
   listeners: Array<EventListenerRegistration>,
   isCapture: boolean,
+  errorState: ListenerErrorState | null,
 ): void {
   for (const listener of listeners) {
     if (listener.removed) {
@@ -454,7 +479,7 @@ function invokeListeners(
         callback.handleEvent(event);
       }
     } catch (error) {
-      reportListenerError(error);
+      handleListenerError(error, errorState);
     }
 
     if (listener.passive) {
@@ -509,12 +534,44 @@ function setEventDispatchFlag(event: Event, value: boolean): void {
   event[EVENT_DISPATCH_FLAG] = value;
 }
 
+type ListenerErrorState = {hasError: boolean, error: unknown};
+
+/**
+ * Handle an error thrown by an event listener without aborting the rest of the
+ * dispatch.
+ *
+ * For trusted dispatch of native UI events (`errorState` is non-null), the
+ * first error is recorded so `dispatch` can rethrow it synchronously once the
+ * dispatch completes, matching the legacy plugin path (React's
+ * runEventsInBatch + `rethrowCaughtError`). This keeps listener errors
+ * catchable by React error boundaries and the native event call, instead of
+ * escaping as deferred uncaught exceptions.
+ *
+ * Otherwise (`errorState` is null: the public `dispatchEvent` API, XHR, etc.)
+ * the DOM spec requires reporting the exception to the global error handler
+ * without throwing, so it is deferred via `reportListenerError`.
+ */
+function handleListenerError(
+  error: unknown,
+  errorState: ListenerErrorState | null,
+): void {
+  if (errorState != null) {
+    if (!errorState.hasError) {
+      errorState.hasError = true;
+      errorState.error = error;
+    }
+    return;
+  }
+
+  reportListenerError(error);
+}
+
 /**
  * Surface a listener error to the global error handler without aborting the
- * rest of the dispatch. Throws in a new task so the error becomes an
- * uncaught exception (matching the legacy plugin path's behavior of
- * propagating listener errors via React's runEventsInBatch +
- * `rethrowCaughtError`, rather than swallowing them as a `console.error`).
+ * rest of the dispatch. Throws in a new task so the error becomes an uncaught
+ * exception. Used for dispatches that follow the DOM `dispatchEvent` contract
+ * (the public API, XHR, etc.), where errors are reported rather than thrown
+ * synchronously.
  *
  * `setTimeout(0)` schedules a new macrotask; the throw inside it has no
  * catcher above, so it bubbles up to the host's unhandled-error reporter.
diff --git a/packages/react-native/src/private/webapis/dom/events/internals/EventTargetInternals.js b/packages/react-native/src/private/webapis/dom/events/internals/EventTargetInternals.js
index 93bf4803feaf..87322c62d1fe 100644
--- a/packages/react-native/src/private/webapis/dom/events/internals/EventTargetInternals.js
+++ b/packages/react-native/src/private/webapis/dom/events/internals/EventTargetInternals.js
@@ -75,13 +75,25 @@ export function getEventTargetParent(target: EventTarget): EventTarget | null {
  *
  * This should only be used by the runtime to dispatch native events to
  * JavaScript.
+ *
+ * When `rethrowListenerErrors` is `true`, the first error thrown by a listener
+ * is rethrown synchronously once dispatch completes (matching the legacy
+ * plugin system's `rethrowCaughtError` behavior). This is used by the renderer
+ * for native UI events so listener errors stay catchable by React error
+ * boundaries and the native event call. When omitted/`false`, listener errors
+ * are reported to the global error handler per the DOM spec (used by XHR and
+ * other web API event targets).
  */
 export function dispatchTrustedEvent(
   eventTarget: EventTarget,
   event: Event,
+  rethrowListenerErrors?: boolean,
 ): boolean {
   setIsTrusted(event, true);
 
   // $FlowExpectedError[prop-missing]
-  return eventTarget[INTERNAL_DISPATCH_METHOD_KEY](event);
+  return eventTarget[INTERNAL_DISPATCH_METHOD_KEY](
+    event,
+    rethrowListenerErrors,
+  );
 }