diff --git a/packages/jest-fake-timers/src/__tests__/modernFakeTimers.test.ts b/packages/jest-fake-timers/src/__tests__/modernFakeTimers.test.ts
index feacc59fec38..3d6d8663540d 100644
--- a/packages/jest-fake-timers/src/__tests__/modernFakeTimers.test.ts
+++ b/packages/jest-fake-timers/src/__tests__/modernFakeTimers.test.ts
@@ -1270,6 +1270,7 @@ describe('FakeTimers', () => {
     });
 
     afterEach(() => {
+      timers.clearAllTimers();
       timers.dispose();
     });
 
@@ -1308,21 +1309,27 @@ describe('FakeTimers', () => {
 
       it('can turn off and on auto advancing of time', async () => {
         let p2Resolved = false;
-        const p1 = new Promise(resolve => global.setTimeout(resolve, 50));
-        const p2 = new Promise(resolve => global.setTimeout(resolve, 51)).then(
-          () => (p2Resolved = true),
-        );
-        const p3 = new Promise(resolve => global.setTimeout(resolve, 52));
+        const p1 = new Promise(resolve => global.setTimeout(resolve, 1));
+        const p2 = new Promise<void>(resolve => global.setTimeout(() => {
+          p2Resolved = true;
+          resolve();
+        }, 2));
+        const p3 = new Promise(resolve => global.setTimeout(resolve, 3));
 
         await expect(p1).resolves.toBeUndefined();
 
         timers.setTickMode('manual');
+        // wait real, unpatched time to ensure p2 doesn't resolve on its own
         await new Promise(resolve => setTimeout(resolve, 5));
         expect(p2Resolved).toBe(false);
 
+        // simply updating the tick mode should not result in time immediately advancing
         timers.setTickMode('nextAsync');
+        expect(p2Resolved).toBe(false);
+
+        // wait real, unpatched time and observe p2 and p3 resolve on their own
         await new Promise(resolve => setTimeout(resolve, 5));
-        await expect(p2).resolves.toBe(true);
+        await expect(p2).resolves.toBeUndefined();
         await expect(p3).resolves.toBeUndefined();
         expect(p2Resolved).toBe(true);
       });
@@ -1340,6 +1347,58 @@ describe('FakeTimers', () => {
         ).toMatchSnapshot();
         consoleWarnSpy.mockRestore();
       });
+
+      describe('works with manual calls to async tick functions', () => {
+        let timerLog: number[];
+        let allTimersDone: Promise<void>;
+        beforeEach(() => {
+          timerLog = [];
+          allTimersDone = new Promise<void>(resolve => {
+            global.setTimeout(() => timerLog.push(1), 1);
+            global.setTimeout(() => timerLog.push(2), 2);
+            global.setTimeout(() => timerLog.push(3), 3);
+            global.setTimeout(() => {
+              timerLog.push(4);
+              global.setTimeout(() => {
+                timerLog.push(5);
+                resolve();
+              }, 1);
+            }, 5);
+          });
+        });
+
+        afterEach(async () => {
+          await allTimersDone;
+          expect(timerLog).toEqual([1, 2, 3, 4, 5]);
+        });
+
+        it('runAllTimersAsync', async () => {
+          await timers.runAllTimersAsync();
+          expect(timerLog).toEqual([1, 2, 3, 4, 5]);
+        });
+
+        it('runOnlyPendingTimersAsync', async () => {
+          await timers.runOnlyPendingTimersAsync();
+          // 5 should not resolve because it wasn't queued when we called "only pending timers"
+          expect(timerLog).toEqual([1, 2, 3, 4]);
+        });
+
+        it('advanceTimersToNextTimerAsync', async () => {
+          await timers.advanceTimersToNextTimerAsync();
+          expect(timerLog).toEqual([1]);
+          await timers.advanceTimersToNextTimerAsync();
+          expect(timerLog).toEqual([1, 2]);
+          await timers.advanceTimersToNextTimerAsync();
+          expect(timerLog).toEqual([1, 2, 3]);
+        });
+
+        it('advanceTimersByTimeAsync', async () => {
+          await timers.advanceTimersByTimeAsync(2);
+          expect(timerLog).toEqual([1, 2]);
+          await timers.advanceTimersByTimeAsync(1);
+          expect(timerLog).toEqual([1, 2, 3]);
+        });
+      });
     });
   });
 
diff --git a/packages/jest-fake-timers/src/modernFakeTimers.ts b/packages/jest-fake-timers/src/modernFakeTimers.ts
index 3f77142dbbb9..4d35d797ffee 100644
--- a/packages/jest-fake-timers/src/modernFakeTimers.ts
+++ b/packages/jest-fake-timers/src/modernFakeTimers.ts
@@ -19,6 +19,7 @@ export type TimerTickMode = 'manual' | 'nextAsync' | 'interval';
 
 export default class FakeTimers {
   private _clock!: InstalledClock;
+  private _nativeTimeout: typeof setTimeout;
   private readonly _config: Config.ProjectConfig;
   private _fakingTime: boolean;
   private _usingSinonAdvanceTime = false;
@@ -38,6 +39,7 @@ export default class FakeTimers {
   }) {
     this._global = global;
     this._config = config;
+    this._nativeTimeout = global.setTimeout;
 
     this._fakingTime = false;
     this._fakeTimers = withGlobal(global);
@@ -61,7 +63,7 @@ export default class FakeTimers {
 
   async runAllTimersAsync(): Promise<void> {
     if (this._checkFakeTimers()) {
-      await this._clock.runAllAsync();
+      await this._runWithoutNextAsyncTickMode(() => this._clock.runAllAsync());
     }
   }
 
@@ -73,7 +75,9 @@ export default class FakeTimers {
 
   async runOnlyPendingTimersAsync(): Promise<void> {
     if (this._checkFakeTimers()) {
-      await this._clock.runToLastAsync();
+      await this._runWithoutNextAsyncTickMode(() =>
+        this._clock.runToLastAsync(),
+      );
     }
   }
 
@@ -94,9 +98,11 @@ export default class FakeTimers {
   async advanceTimersToNextTimerAsync(steps = 1): Promise<void> {
     if (this._checkFakeTimers()) {
       for (let i = steps; i > 0; i--) {
-        await this._clock.nextAsync();
-        // Fire all timers at this point: https://github.com/sinonjs/fake-timers/issues/250
-        await this._clock.tickAsync(0);
+        await this._runWithoutNextAsyncTickMode(async () => {
+          await this._clock.nextAsync();
+          // Fire all timers at this point: https://github.com/sinonjs/fake-timers/issues/250
+          await this._clock.tickAsync(0);
+        });
 
         if (this._clock.countTimers() === 0) {
           break;
@@ -113,7 +119,9 @@ export default class FakeTimers {
 
   async advanceTimersByTimeAsync(msToRun: number): Promise<void> {
     if (this._checkFakeTimers()) {
-      await this._clock.tickAsync(msToRun);
+      await this._runWithoutNextAsyncTickMode(() =>
+        this._clock.tickAsync(msToRun),
+      );
     }
   }
 
@@ -297,10 +305,29 @@ export default class FakeTimers {
     }
     const {counter} = this.tickMode;
 
+    // Wait a macrotask to prevent advancing time immediately when
+    await new Promise(resolve => void this._nativeTimeout(resolve));
     while (this.tickMode.counter === counter && this._fakingTime) {
       // nextAsync always resolves in a setTimeout, even when there are no timers.
       // https://github.com/sinonjs/fake-timers/blob/710cafad25abe9465c807efd8ed9cf3a15985fb1/src/fake-timers-src.js#L1517-L1546
       await this._clock.nextAsync();
     }
   }
+
+  /**
+   * Temporarily disables the `nextAsync` tick mode while the given function
+   * executes. Used to prevent the auto-advance from advancing while the
+   * user is waiting for a manually requested async tick.
+   */
+  private async _runWithoutNextAsyncTickMode(fn: () => Promise<unknown>) {
+    let resetModeToNextAsync = false;
+    if (this.tickMode.mode === 'nextAsync') {
+      this.setTickMode('manual');
+      resetModeToNextAsync = true;
+    }
+    await fn();
+    if (resetModeToNextAsync) {
+      this.setTickMode('nextAsync');
+    }
+  }
 }