diff --git a/packages/cli-repl/src/mongosh-repl.spec.ts b/packages/cli-repl/src/mongosh-repl.spec.ts
index 4c05a3581..8ac61b058 100644
--- a/packages/cli-repl/src/mongosh-repl.spec.ts
+++ b/packages/cli-repl/src/mongosh-repl.spec.ts
@@ -23,6 +23,11 @@ import MongoshNodeRepl from './mongosh-repl';
 import { parseAnyLogEntry } from '../../shell-api/src/log-entry';
 import stripAnsi from 'strip-ansi';
 
+function nonnull<T>(value: T | null | undefined): NonNullable<T> {
+  if (!value) throw new Error();
+  return value;
+}
+
 const delay = promisify(setTimeout);
 
 const multilineCode = `(function() {
@@ -280,7 +285,7 @@ describe('MongoshNodeRepl', function () {
     it('handles a long series of errors', async function () {
       input.write('-asdf();\n'.repeat(20));
       await waitEval(bus);
-      expect(mongoshRepl.runtimeState().repl.listenerCount('SIGINT')).to.equal(
+      expect(mongoshRepl.runtimeState().repl?.listenerCount('SIGINT')).to.equal(
         1
       );
     });
@@ -548,7 +553,7 @@ describe('MongoshNodeRepl', function () {
             await tick();
             input.write('"bar" })\n');
             await tick();
-            expect(mongoshRepl.runtimeState().repl.context.obj).to.deep.equal({
+            expect(mongoshRepl.runtimeState().context.obj).to.deep.equal({
               foo: 'bar',
             });
             expect(output).not.to.include('obj = ({ foo: "bar" })');
@@ -571,7 +576,7 @@ describe('MongoshNodeRepl', function () {
             await tick();
             input.write('\u0004'); // Ctrl+D
             await tick();
-            expect(mongoshRepl.runtimeState().repl.context.obj).to.deep.equal({
+            expect(mongoshRepl.runtimeState().context.obj).to.deep.equal({
               foo: 'baz',
             });
             expect(output).not.to.include('obj = ({ foo: "baz" })');
@@ -596,7 +601,7 @@ describe('MongoshNodeRepl', function () {
             await tick();
             input.write('"bar" })\n');
             await tick();
-            expect(mongoshRepl.runtimeState().repl.context.obj).to.deep.equal({
+            expect(mongoshRepl.runtimeState().context.obj).to.deep.equal({
               foo: 'bar',
             });
             expect(output).not.to.include('obj = ({ foo: "bar" })');
@@ -638,7 +643,10 @@ describe('MongoshNodeRepl', function () {
 
           it('does not crash if hitting enter and then up', async function () {
             input.write('\n');
-            await once(mongoshRepl.runtimeState().repl, 'flushHistory');
+            await once(
+              nonnull(mongoshRepl.runtimeState().repl),
+              'flushHistory'
+            );
             input.write(`${arrowUp}`);
             await tick();
           });
@@ -646,11 +654,20 @@ describe('MongoshNodeRepl', function () {
           context('redaction', function () {
             it('removes sensitive commands by default', async function () {
               input.write('connect\n');
-              await once(mongoshRepl.runtimeState().repl, 'flushHistory');
+              await once(
+                nonnull(mongoshRepl.runtimeState().repl),
+                'flushHistory'
+              );
               input.write('connection\n');
-              await once(mongoshRepl.runtimeState().repl, 'flushHistory');
+              await once(
+                nonnull(mongoshRepl.runtimeState().repl),
+                'flushHistory'
+              );
               input.write('db.test.insert({ email: "foo@example.org" })\n');
-              await once(mongoshRepl.runtimeState().repl, 'flushHistory');
+              await once(
+                nonnull(mongoshRepl.runtimeState().repl),
+                'flushHistory'
+              );
 
               expect(getHistory()).to.deep.equal([
                 'db.test.insert({ email: "foo@example.org" })',
@@ -662,11 +679,20 @@ describe('MongoshNodeRepl', function () {
               input.write('config.set("redactHistory", "keep");\n');
               await tick();
               input.write('connect\n');
-              await once(mongoshRepl.runtimeState().repl, 'flushHistory');
+              await once(
+                nonnull(mongoshRepl.runtimeState().repl),
+                'flushHistory'
+              );
               input.write('connection\n');
-              await once(mongoshRepl.runtimeState().repl, 'flushHistory');
+              await once(
+                nonnull(mongoshRepl.runtimeState().repl),
+                'flushHistory'
+              );
               input.write('db.test.insert({ email: "foo@example.org" })\n');
-              await once(mongoshRepl.runtimeState().repl, 'flushHistory');
+              await once(
+                nonnull(mongoshRepl.runtimeState().repl),
+                'flushHistory'
+              );
 
               expect(getHistory()).to.deep.equal([
                 'db.test.insert({ email: "foo@example.org" })',
@@ -680,11 +706,20 @@ describe('MongoshNodeRepl', function () {
               input.write('config.set("redactHistory", "remove-redact");\n');
               await tick();
               input.write('connect\n');
-              await once(mongoshRepl.runtimeState().repl, 'flushHistory');
+              await once(
+                nonnull(mongoshRepl.runtimeState().repl),
+                'flushHistory'
+              );
               input.write('connection\n');
-              await once(mongoshRepl.runtimeState().repl, 'flushHistory');
+              await once(
+                nonnull(mongoshRepl.runtimeState().repl),
+                'flushHistory'
+              );
               input.write('db.test.insert({ email: "foo@example.org" })\n');
-              await once(mongoshRepl.runtimeState().repl, 'flushHistory');
+              await once(
+                nonnull(mongoshRepl.runtimeState().repl),
+                'flushHistory'
+              );
 
               expect(getHistory()).to.deep.equal([
                 'db.test.insert({ email: "<email>" })',
@@ -783,11 +818,9 @@ describe('MongoshNodeRepl', function () {
 
     it('does not refresh the prompt if a window resize occurs while evaluating', async function () {
       let resolveInProgress;
-      mongoshRepl.runtimeState().repl.context.inProgress = new Promise(
-        (resolve) => {
-          resolveInProgress = resolve;
-        }
-      );
+      mongoshRepl.runtimeState().context.inProgress = new Promise((resolve) => {
+        resolveInProgress = resolve;
+      });
       input.write('inProgress\n');
       await tick();
 
@@ -887,7 +920,7 @@ describe('MongoshNodeRepl', function () {
     context('user prompts', function () {
       beforeEach(function () {
         // No boolean equivalent for 'passwordPrompt' in the API, so provide one:
-        mongoshRepl.runtimeState().repl.context.booleanPrompt = (question) => {
+        mongoshRepl.runtimeState().context.booleanPrompt = (question) => {
           return Object.assign(mongoshRepl.onPrompt(question, 'yesno'), {
             [Symbol.for('@@mongosh.syntheticPromise')]: true,
           });
@@ -1283,6 +1316,29 @@ describe('MongoshNodeRepl', function () {
         expect(output).to.contain('> ');
       });
     });
+
+    context('pre-specified user-provided prompt', function () {
+      it('does not attempt to run the prompt in parallel with initial input', async function () {
+        output = '';
+        const initialized = await mongoshRepl.initialize(serviceProvider);
+        await mongoshRepl.loadExternalCode(
+          `prompt = () => {
+          if (globalThis.isEvaluating) print('FAILED -- Parallel execution detected!');
+          globalThis.isEvaluating = true;
+          sleep(100);
+          globalThis.isEvaluating = false;
+          return '> ';
+        };`,
+          'test'
+        );
+        expect(mongoshRepl.runtimeState().context.prompt).to.be.a('function');
+        // Queue up input *before* starting the REPL itself
+        input.write('prompt()\n');
+        await mongoshRepl.startRepl(initialized);
+        await waitEval(bus);
+        expect(output).not.to.include('FAILED');
+      });
+    });
   });
 
   context('before the REPL starts', function () {
diff --git a/packages/cli-repl/src/mongosh-repl.ts b/packages/cli-repl/src/mongosh-repl.ts
index 325f2eaed..baa8ce0e7 100644
--- a/packages/cli-repl/src/mongosh-repl.ts
+++ b/packages/cli-repl/src/mongosh-repl.ts
@@ -533,11 +533,13 @@ class MongoshNodeRepl implements EvaluationListener {
         'Cannot start REPL when not in REPL evaluation mode'
       );
     }
+    // Set up the prompt before consuming input so that we do not end up
+    // running the prompt function in parallel with actual input code.
+    repl.setPrompt(await this.getShellPrompt());
     // Only start reading from the input *after* we set up everything, including
-    // instanceState.setCtx().
+    // instanceState.setCtx() and configuring the REPL prompt.
     this.lineByLineInput.start();
     this.input.resume();
-    repl.setPrompt(await this.getShellPrompt());
     repl.displayPrompt();
   }
 
diff --git a/packages/e2e-tests/test/e2e.spec.ts b/packages/e2e-tests/test/e2e.spec.ts
index 649369260..9f6bfdcc3 100644
--- a/packages/e2e-tests/test/e2e.spec.ts
+++ b/packages/e2e-tests/test/e2e.spec.ts
@@ -262,6 +262,26 @@ describe('e2e', function () {
       }
       expect(buffer).to.include('"i": 99999');
     });
+    it('handles custom prompt() function in conjunction with line-by-line input well', async function () {
+      // https://jira.mongodb.org/browse/MONGOSH-1617
+      shell = TestShell.start({
+        args: [
+          '--nodb',
+          '--shell',
+          '--eval',
+          'prompt = () => {sleep(1);return "x>"}',
+        ],
+      });
+      // The number of newlines here matters
+      shell.writeInput(
+        'sleep(100);print([1,2,3,4,5,6,7,8,9,10].reduce(\n(a,b) => { return a*b; }, 1))\n\n\n\n',
+        { end: true }
+      );
+      const exitCode = await shell.waitForExit();
+      expect(exitCode).to.equal(0);
+      shell.assertContainsOutput('3628800');
+      shell.assertNoErrors();
+    });
   });
 
   describe('set db', function () {
@@ -1035,6 +1055,25 @@ describe('e2e', function () {
         shell.assertContainsOutput('admin;system.version;');
       });
     });
+
+    it('works fine with custom prompts', async function () {
+      // https://jira.mongodb.org/browse/MONGOSH-1617
+      shell = TestShell.start({
+        args: [
+          await testServer.connectionString(),
+          '--eval',
+          'prompt = () => db.stats().db',
+          '--shell',
+        ],
+      });
+      shell.writeInput(
+        '[db.hello()].reduce(\n() => { return 11111*11111; },0)\n\n\n',
+        { end: true }
+      );
+      await shell.waitForExit();
+      shell.assertContainsOutput('123454321');
+      shell.assertNoErrors();
+    });
   });
 
   describe('Node.js builtin APIs in the shell', function () {
diff --git a/packages/e2e-tests/test/test-shell.ts b/packages/e2e-tests/test/test-shell.ts
index a274e1b29..9cf384b88 100644
--- a/packages/e2e-tests/test/test-shell.ts
+++ b/packages/e2e-tests/test/test-shell.ts
@@ -215,8 +215,9 @@ export class TestShell {
     this._process.kill(signal);
   }
 
-  writeInput(chars: string): void {
+  writeInput(chars: string, { end = false } = {}): void {
     this._process.stdin.write(chars);
+    if (end) this._process.stdin.end();
   }
 
   writeInputLine(chars: string): void {