diff --git a/packages/cli-repl/src/async-repl.ts b/packages/cli-repl/src/async-repl.ts
index 175d9e86fb..2566a1bf20 100644
--- a/packages/cli-repl/src/async-repl.ts
+++ b/packages/cli-repl/src/async-repl.ts
@@ -49,7 +49,12 @@ function disableEvent(emitter: EventEmitter, event: string): RestoreEvents {
   };
 }
 
-// Start a REPLSever that supports asynchronous evaluation, rather than just
+function getPrompt(repl: any): string {
+  // Use public getPrompt() API once available (Node.js 15+)
+  return repl.getPrompt?.() ?? repl._prompt;
+}
+
+// Start a REPLServer that supports asynchronous evaluation, rather than just
 // synchronous, and integrates nicely with Ctrl+C handling in that respect.
 export function start(opts: AsyncREPLOptions): REPLServer {
   const repl = (opts.start ?? originalStart)(opts);
@@ -64,6 +69,10 @@ export function start(opts: AsyncREPLOptions): REPLServer {
     let result;
     repl.emit(evalStart, { input } as EvalStartEvent);
 
+    // Use public getPrompt() API once available (Node.js 15+)
+    const origPrompt = getPrompt(repl);
+    repl.setPrompt(''); // Disable printing prompts while we're evaluating code.
+
     try {
       let exitEventPending = false;
       const exitListener = () => { exitEventPending = true; };
@@ -116,6 +125,10 @@ export function start(opts: AsyncREPLOptions): REPLServer {
         (replSigint as any)?.restore?.();
         (processSigint as any)?.restore?.();
 
+        if (getPrompt(repl) === '') {
+          repl.setPrompt(origPrompt);
+        }
+
         repl.removeListener('exit', exitListener);
         for (const listener of previousExitListeners) {
           repl.on('exit', listener);
diff --git a/packages/cli-repl/src/mongosh-repl.spec.ts b/packages/cli-repl/src/mongosh-repl.spec.ts
index 1d2a38a883..7b8852ff93 100644
--- a/packages/cli-repl/src/mongosh-repl.spec.ts
+++ b/packages/cli-repl/src/mongosh-repl.spec.ts
@@ -453,6 +453,35 @@ describe('MongoshNodeRepl', () => {
         expect(history).to.have.lengthOf(2);
       });
     });
+
+    it('refreshes the prompt if a window resize occurs', async() => {
+      output = '';
+      outputStream.emit('resize');
+      await tick();
+      expect(stripAnsi(output)).to.equal('> ');
+    });
+
+    it('does not refresh the prompt if a window resize occurs while evaluating', async() => {
+      let resolveInProgress;
+      mongoshRepl.runtimeState().repl.context.inProgress =
+        new Promise(resolve => { resolveInProgress = resolve; });
+      input.write('inProgress\n');
+      await tick();
+
+      output = '';
+      outputStream.emit('resize');
+      await tick();
+      // The empty space is because the Node.js readline implementation still
+      // tries to make sure that something is printed when a resize happens.
+      // This is okay, though, because it also moves the cursor back to where
+      // it originally was.
+      expect(stripAnsi(output)).to.equal(' ');
+
+      output = '';
+      resolveInProgress();
+      await tick();
+      expect(stripAnsi(output)).to.equal('\n> ');
+    });
   });
 
   context('with fake TTY', () => {