diff --git a/packages/react-dom/src/__tests__/ReactDOMFizzServer-test.js b/packages/react-dom/src/__tests__/ReactDOMFizzServer-test.js
index 72ed9f8775dab..070d71dd89ec7 100644
--- a/packages/react-dom/src/__tests__/ReactDOMFizzServer-test.js
+++ b/packages/react-dom/src/__tests__/ReactDOMFizzServer-test.js
@@ -2850,8 +2850,83 @@ describe('ReactDOMFizzServer', () => {
     });
   });
 
+  it('#24384: Suspending should halt hydration warnings and not emit any if hydration completes successfully after unsuspending', async () => {
+    const makeApp = () => {
+      let resolve, resolved;
+      const promise = new Promise(r => {
+        resolve = () => {
+          resolved = true;
+          return r();
+        };
+      });
+      function ComponentThatSuspends() {
+        if (!resolved) {
+          throw promise;
+        }
+        return <p>A</p>;
+      }
+
+      const App = () => {
+        return (
+          <div>
+            <Suspense fallback={<h1>Loading...</h1>}>
+              <ComponentThatSuspends />
+              <h2 name="hello">world</h2>
+            </Suspense>
+          </div>
+        );
+      };
+
+      return [App, resolve];
+    };
+
+    const [ServerApp, serverResolve] = makeApp();
+    await act(async () => {
+      const {pipe} = ReactDOMFizzServer.renderToPipeableStream(<ServerApp />);
+      pipe(writable);
+    });
+    await act(() => {
+      serverResolve();
+    });
+
+    expect(getVisibleChildren(container)).toEqual(
+      <div>
+        <p>A</p>
+        <h2 name="hello">world</h2>
+      </div>,
+    );
+
+    const [ClientApp, clientResolve] = makeApp();
+    ReactDOMClient.hydrateRoot(container, <ClientApp />, {
+      onRecoverableError(error) {
+        Scheduler.unstable_yieldValue(
+          'Logged recoverable error: ' + error.message,
+        );
+      },
+    });
+    Scheduler.unstable_flushAll();
+
+    expect(getVisibleChildren(container)).toEqual(
+      <div>
+        <p>A</p>
+        <h2 name="hello">world</h2>
+      </div>,
+    );
+
+    // Now that the boundary resolves to it's children the hydration completes and discovers that there is a mismatch requiring
+    // client-side rendering.
+    await clientResolve();
+    expect(Scheduler).toFlushWithoutYielding();
+    expect(getVisibleChildren(container)).toEqual(
+      <div>
+        <p>A</p>
+        <h2 name="hello">world</h2>
+      </div>,
+    );
+  });
+
   // @gate experimental && enableClientRenderFallbackOnTextMismatch
-  it('#24384: Suspending should halt hydration warnings while still allowing siblings to warm up', async () => {
+  it('#24384: Suspending should halt hydration warnings but still emit hydration warnings after unsuspending if mismatches are genuine', async () => {
     const makeApp = () => {
       let resolve, resolved;
       const promise = new Promise(r => {
@@ -3092,4 +3167,367 @@ describe('ReactDOMFizzServer', () => {
 
     expect(Scheduler).toFlushAndYield([]);
   });
+
+  // @gate experimental && __DEV__
+  it('does not invokeGuardedCallback for errors after the first hydration error', async () => {
+    // We can't use the toErrorDev helper here because this is async.
+    const originalConsoleError = console.error;
+    const mockError = jest.fn();
+    console.error = (...args) => {
+      if (args.length > 1) {
+        if (typeof args[1] === 'object') {
+          mockError(args[0].split('\n')[0]);
+          return;
+        }
+      }
+      mockError(...args.map(normalizeCodeLocInfo));
+    };
+    let isClient = false;
+    let shouldThrow = true;
+
+    function ThrowUntilOnClient({children, message}) {
+      if (isClient && shouldThrow) {
+        Scheduler.unstable_yieldValue('throwing: ' + message);
+        throw new Error(message);
+      }
+      return children;
+    }
+
+    function StopThrowingOnClient() {
+      if (isClient) {
+        shouldThrow = false;
+      }
+      return null;
+    }
+
+    const App = () => {
+      return (
+        <div>
+          <Suspense fallback={<h1>Loading...</h1>}>
+            <ThrowUntilOnClient message="first error">
+              <h1>one</h1>
+            </ThrowUntilOnClient>
+            <ThrowUntilOnClient message="second error">
+              <h2>two</h2>
+            </ThrowUntilOnClient>
+            <ThrowUntilOnClient message="third error">
+              <h3>three</h3>
+            </ThrowUntilOnClient>
+            <StopThrowingOnClient />
+          </Suspense>
+        </div>
+      );
+    };
+
+    try {
+      await act(async () => {
+        const {pipe} = ReactDOMFizzServer.renderToPipeableStream(<App />);
+        pipe(writable);
+      });
+
+      expect(getVisibleChildren(container)).toEqual(
+        <div>
+          <h1>one</h1>
+          <h2>two</h2>
+          <h3>three</h3>
+        </div>,
+      );
+
+      isClient = true;
+
+      ReactDOMClient.hydrateRoot(container, <App />, {
+        onRecoverableError(error) {
+          Scheduler.unstable_yieldValue(
+            'Logged recoverable error: ' + error.message,
+          );
+        },
+      });
+      expect(Scheduler).toFlushAndYield([
+        'throwing: first error',
+        // this repeated first error is the invokeGuardedCallback throw
+        'throwing: first error',
+        // these are actually thrown during render but no iGC repeat and no queueing as hydration errors
+        'throwing: second error',
+        'throwing: third error',
+        // all hydration errors are still queued
+        'Logged recoverable error: first error',
+        'Logged recoverable error: second error',
+        'Logged recoverable error: third error',
+        // other recoverable errors are queued as hydration errors
+        'Logged recoverable error: There was an error while hydrating this Suspense boundary. Switched to client rendering.',
+      ]);
+      // These Uncaught error calls are the error reported by the runtime (jsdom here, browser in actual use)
+      // when invokeGuardedCallback is used to replay an error in dev using event dispatching in the document
+      expect(mockError.mock.calls).toEqual([
+        // we only get one because we suppress invokeGuardedCallback after the first one when hydrating in a
+        // suspense boundary
+        ['Error: Uncaught [Error: first error]'],
+      ]);
+      mockError.mockClear();
+
+      expect(getVisibleChildren(container)).toEqual(
+        <div>
+          <h1>one</h1>
+          <h2>two</h2>
+          <h3>three</h3>
+        </div>,
+      );
+
+      expect(Scheduler).toFlushAndYield([]);
+      expect(mockError.mock.calls).toEqual([]);
+    } finally {
+      console.error = originalConsoleError;
+    }
+  });
+
+  // @gate experimental
+  it('does not invokeGuardedCallback for errors after a preceding fiber suspends', async () => {
+    // We can't use the toErrorDev helper here because this is async.
+    const originalConsoleError = console.error;
+    const mockError = jest.fn();
+    console.error = (...args) => {
+      if (args.length > 1) {
+        if (typeof args[1] === 'object') {
+          mockError(args[0].split('\n')[0]);
+          return;
+        }
+      }
+      mockError(...args.map(normalizeCodeLocInfo));
+    };
+    let isClient = false;
+    let shouldThrow = true;
+    let promise = null;
+    let unsuspend = null;
+    let isResolved = false;
+
+    function ComponentThatSuspendsOnClient() {
+      if (isClient && !isResolved) {
+        if (promise === null) {
+          promise = new Promise(resolve => {
+            unsuspend = () => {
+              isResolved = true;
+              resolve();
+            };
+          });
+        }
+        Scheduler.unstable_yieldValue('suspending');
+        throw promise;
+      }
+      return null;
+    }
+
+    function ThrowUntilOnClient({children, message}) {
+      if (isClient && shouldThrow) {
+        Scheduler.unstable_yieldValue('throwing: ' + message);
+        throw new Error(message);
+      }
+      return children;
+    }
+
+    function StopThrowingOnClient() {
+      if (isClient) {
+        shouldThrow = false;
+      }
+      return null;
+    }
+
+    const App = () => {
+      return (
+        <div>
+          <Suspense fallback={<h1>Loading...</h1>}>
+            <ComponentThatSuspendsOnClient />
+            <ThrowUntilOnClient message="first error">
+              <h1>one</h1>
+            </ThrowUntilOnClient>
+            <ThrowUntilOnClient message="second error">
+              <h2>two</h2>
+            </ThrowUntilOnClient>
+            <ThrowUntilOnClient message="third error">
+              <h3>three</h3>
+            </ThrowUntilOnClient>
+            <StopThrowingOnClient />
+          </Suspense>
+        </div>
+      );
+    };
+
+    try {
+      await act(async () => {
+        const {pipe} = ReactDOMFizzServer.renderToPipeableStream(<App />);
+        pipe(writable);
+      });
+
+      expect(getVisibleChildren(container)).toEqual(
+        <div>
+          <h1>one</h1>
+          <h2>two</h2>
+          <h3>three</h3>
+        </div>,
+      );
+
+      isClient = true;
+
+      ReactDOMClient.hydrateRoot(container, <App />, {
+        onRecoverableError(error) {
+          Scheduler.unstable_yieldValue(
+            'Logged recoverable error: ' + error.message,
+          );
+        },
+      });
+      expect(Scheduler).toFlushAndYield([
+        'suspending',
+        'throwing: first error',
+        // There is no repeated first error because we already suspended and no
+        // invokeGuardedCallback is used if we are in dev
+        // or in prod there is just never an invokeGuardedCallback
+        'throwing: second error',
+        'throwing: third error',
+      ]);
+      expect(mockError.mock.calls).toEqual([]);
+
+      expect(getVisibleChildren(container)).toEqual(
+        <div>
+          <h1>one</h1>
+          <h2>two</h2>
+          <h3>three</h3>
+        </div>,
+      );
+      await unsuspend();
+      // Since our client components only throw on the very first render there are no
+      // new throws in this pass
+      expect(Scheduler).toFlushAndYield([]);
+
+      expect(mockError.mock.calls).toEqual([]);
+    } finally {
+      console.error = originalConsoleError;
+    }
+  });
+
+  // @gate experimental && __DEV__
+  it('suspending after erroring will cause errors previously queued to be silenced until the boundary resolves', async () => {
+    // We can't use the toErrorDev helper here because this is async.
+    const originalConsoleError = console.error;
+    const mockError = jest.fn();
+    console.error = (...args) => {
+      if (args.length > 1) {
+        if (typeof args[1] === 'object') {
+          mockError(args[0].split('\n')[0]);
+          return;
+        }
+      }
+      mockError(...args.map(normalizeCodeLocInfo));
+    };
+    let isClient = false;
+    let shouldThrow = true;
+    let promise = null;
+    let unsuspend = null;
+    let isResolved = false;
+
+    function ComponentThatSuspendsOnClient() {
+      if (isClient && !isResolved) {
+        if (promise === null) {
+          promise = new Promise(resolve => {
+            unsuspend = () => {
+              isResolved = true;
+              resolve();
+            };
+          });
+        }
+        Scheduler.unstable_yieldValue('suspending');
+        throw promise;
+      }
+      return null;
+    }
+
+    function ThrowUntilOnClient({children, message}) {
+      if (isClient && shouldThrow) {
+        Scheduler.unstable_yieldValue('throwing: ' + message);
+        throw new Error(message);
+      }
+      return children;
+    }
+
+    function StopThrowingOnClient() {
+      if (isClient) {
+        shouldThrow = false;
+      }
+      return null;
+    }
+
+    const App = () => {
+      return (
+        <div>
+          <Suspense fallback={<h1>Loading...</h1>}>
+            <ThrowUntilOnClient message="first error">
+              <h1>one</h1>
+            </ThrowUntilOnClient>
+            <ThrowUntilOnClient message="second error">
+              <h2>two</h2>
+            </ThrowUntilOnClient>
+            <ComponentThatSuspendsOnClient />
+            <ThrowUntilOnClient message="third error">
+              <h3>three</h3>
+            </ThrowUntilOnClient>
+            <StopThrowingOnClient />
+          </Suspense>
+        </div>
+      );
+    };
+
+    try {
+      await act(async () => {
+        const {pipe} = ReactDOMFizzServer.renderToPipeableStream(<App />);
+        pipe(writable);
+      });
+
+      expect(getVisibleChildren(container)).toEqual(
+        <div>
+          <h1>one</h1>
+          <h2>two</h2>
+          <h3>three</h3>
+        </div>,
+      );
+
+      isClient = true;
+
+      ReactDOMClient.hydrateRoot(container, <App />, {
+        onRecoverableError(error) {
+          Scheduler.unstable_yieldValue(
+            'Logged recoverable error: ' + error.message,
+          );
+        },
+      });
+      expect(Scheduler).toFlushAndYield([
+        'throwing: first error',
+        // duplicate because first error is re-done in invokeGuardedCallback
+        'throwing: first error',
+        'throwing: second error',
+        'suspending',
+        'throwing: third error',
+      ]);
+      // These Uncaught error calls are the error reported by the runtime (jsdom here, browser in actual use)
+      // when invokeGuardedCallback is used to replay an error in dev using event dispatching in the document
+      expect(mockError.mock.calls).toEqual([
+        // we only get one because we suppress invokeGuardedCallback after the first one when hydrating in a
+        // suspense boundary
+        ['Error: Uncaught [Error: first error]'],
+      ]);
+      mockError.mockClear();
+
+      expect(getVisibleChildren(container)).toEqual(
+        <div>
+          <h1>one</h1>
+          <h2>two</h2>
+          <h3>three</h3>
+        </div>,
+      );
+      await unsuspend();
+      // Since our client components only throw on the very first render there are no
+      // new throws in this pass
+      expect(Scheduler).toFlushAndYield([]);
+      expect(mockError.mock.calls).toEqual([]);
+    } finally {
+      console.error = originalConsoleError;
+    }
+  });
 });
diff --git a/packages/react-reconciler/src/ReactFiberHydrationContext.new.js b/packages/react-reconciler/src/ReactFiberHydrationContext.new.js
index e0e592d32790f..636a467475df4 100644
--- a/packages/react-reconciler/src/ReactFiberHydrationContext.new.js
+++ b/packages/react-reconciler/src/ReactFiberHydrationContext.new.js
@@ -104,6 +104,13 @@ export function markDidThrowWhileHydratingDEV() {
   }
 }
 
+export function didSuspendOrErrorWhileHydratingDEV() {
+  if (__DEV__) {
+    return didSuspendOrErrorDEV;
+  }
+  return false;
+}
+
 function enterHydrationState(fiber: Fiber): boolean {
   if (!supportsHydration) {
     return false;
diff --git a/packages/react-reconciler/src/ReactFiberHydrationContext.old.js b/packages/react-reconciler/src/ReactFiberHydrationContext.old.js
index a4fd5c93e22ea..3befb348c05ab 100644
--- a/packages/react-reconciler/src/ReactFiberHydrationContext.old.js
+++ b/packages/react-reconciler/src/ReactFiberHydrationContext.old.js
@@ -104,6 +104,13 @@ export function markDidThrowWhileHydratingDEV() {
   }
 }
 
+export function didSuspendOrErrorWhileHydratingDEV() {
+  if (__DEV__) {
+    return didSuspendOrErrorDEV;
+  }
+  return false;
+}
+
 function enterHydrationState(fiber: Fiber): boolean {
   if (!supportsHydration) {
     return false;
diff --git a/packages/react-reconciler/src/ReactFiberWorkLoop.new.js b/packages/react-reconciler/src/ReactFiberWorkLoop.new.js
index 89c880d868554..b4343485259ae 100644
--- a/packages/react-reconciler/src/ReactFiberWorkLoop.new.js
+++ b/packages/react-reconciler/src/ReactFiberWorkLoop.new.js
@@ -88,6 +88,7 @@ import {
   assignFiberPropertiesInDEV,
 } from './ReactFiber.new';
 import {isRootDehydrated} from './ReactFiberShellHydration';
+import {didSuspendOrErrorWhileHydratingDEV} from './ReactFiberHydrationContext.new';
 import {NoMode, ProfileMode, ConcurrentMode} from './ReactTypeOfMode';
 import {
   HostRoot,
@@ -3001,11 +3002,13 @@ if (__DEV__ && replayFailedUnitOfWorkWithInvokeGuardedCallback) {
       return originalBeginWork(current, unitOfWork, lanes);
     } catch (originalError) {
       if (
-        originalError !== null &&
-        typeof originalError === 'object' &&
-        typeof originalError.then === 'function'
+        didSuspendOrErrorWhileHydratingDEV() ||
+        (originalError !== null &&
+          typeof originalError === 'object' &&
+          typeof originalError.then === 'function')
       ) {
-        // Don't replay promises. Treat everything else like an error.
+        // Don't replay promises.
+        // Don't replay errors if we are hydrating and have already suspended or handled an error
         throw originalError;
       }
 
diff --git a/packages/react-reconciler/src/ReactFiberWorkLoop.old.js b/packages/react-reconciler/src/ReactFiberWorkLoop.old.js
index 2f5dbe8530ce5..58757a37367ce 100644
--- a/packages/react-reconciler/src/ReactFiberWorkLoop.old.js
+++ b/packages/react-reconciler/src/ReactFiberWorkLoop.old.js
@@ -88,6 +88,7 @@ import {
   assignFiberPropertiesInDEV,
 } from './ReactFiber.old';
 import {isRootDehydrated} from './ReactFiberShellHydration';
+import {didSuspendOrErrorWhileHydratingDEV} from './ReactFiberHydrationContext.old';
 import {NoMode, ProfileMode, ConcurrentMode} from './ReactTypeOfMode';
 import {
   HostRoot,
@@ -3001,11 +3002,13 @@ if (__DEV__ && replayFailedUnitOfWorkWithInvokeGuardedCallback) {
       return originalBeginWork(current, unitOfWork, lanes);
     } catch (originalError) {
       if (
-        originalError !== null &&
-        typeof originalError === 'object' &&
-        typeof originalError.then === 'function'
+        didSuspendOrErrorWhileHydratingDEV() ||
+        (originalError !== null &&
+          typeof originalError === 'object' &&
+          typeof originalError.then === 'function')
       ) {
-        // Don't replay promises. Treat everything else like an error.
+        // Don't replay promises.
+        // Don't replay errors if we are hydrating and have already suspended or handled an error
         throw originalError;
       }