diff --git a/CHANGELOG.md b/CHANGELOG.md
index ff406166c692..db63ad8a0581 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -20,6 +20,7 @@
 - `[jest-cli]` Improve the message when running coverage while there are no files matching global threshold ([#6334](https://github.com/facebook/jest/pull/6334))
 - `[jest-snapshot]` Correctly merge property matchers with the rest of the snapshot in `toMatchSnapshot`. ([#6528](https://github.com/facebook/jest/pull/6528))
 - `[jest-snapshot]` Add error messages for invalid property matchers. ([#6528](https://github.com/facebook/jest/pull/6528))
+- `[jest-cli]` Show open handles from inside test files as well ([#6263](https://github.com/facebook/jest/pull/6263))
 
 ### Chore & Maintenance
 
diff --git a/e2e/__tests__/__snapshots__/detect_open_handles.js.snap b/e2e/__tests__/__snapshots__/detect_open_handles.js.snap
index 10de6b087412..994c7f7d38b0 100644
--- a/e2e/__tests__/__snapshots__/detect_open_handles.js.snap
+++ b/e2e/__tests__/__snapshots__/detect_open_handles.js.snap
@@ -11,3 +11,18 @@ exports[`prints message about flag on slow tests 1`] = `
 
 This usually means that there are asynchronous operations that weren't stopped in your tests. Consider running Jest with \`--detectOpenHandles\` to troubleshoot this issue."
 `;
+
+exports[`prints out info about open handlers from inside tests 1`] = `
+"Jest has detected the following 1 open handle potentially keeping Jest from exiting:
+
+  ●  Timeout
+
+      1 | test('something', () => {
+    > 2 |   setTimeout(() => {}, 30000);
+        |   ^
+      3 |   expect(true).toBe(true);
+      4 | });
+      5 | 
+
+      at Object.<anonymous>.test (__tests__/inside.js:2:3)"
+`;
diff --git a/e2e/__tests__/detect_open_handles.js b/e2e/__tests__/detect_open_handles.js
index 51e4059d7084..3e0081326531 100644
--- a/e2e/__tests__/detect_open_handles.js
+++ b/e2e/__tests__/detect_open_handles.js
@@ -85,3 +85,14 @@ it('does not report promises', () => {
 
   expect(textAfterTest).toBe('');
 });
+
+it('prints out info about open handlers from inside tests', async () => {
+  const {stderr} = await runJest.until(
+    'detect-open-handles',
+    ['inside', '--detectOpenHandles'],
+    'Jest has detected',
+  );
+  const textAfterTest = getTextAfterTest(stderr);
+
+  expect(textAfterTest).toMatchSnapshot();
+});
diff --git a/e2e/detect-open-handles/__tests__/inside.js b/e2e/detect-open-handles/__tests__/inside.js
new file mode 100644
index 000000000000..5b1c0d5b3c1d
--- /dev/null
+++ b/e2e/detect-open-handles/__tests__/inside.js
@@ -0,0 +1,4 @@
+test('something', () => {
+  setTimeout(() => {}, 30000);
+  expect(true).toBe(true);
+});
diff --git a/packages/jest-circus/src/run.js b/packages/jest-circus/src/run.js
index 1a05d7e45834..bf6bae4f2683 100644
--- a/packages/jest-circus/src/run.js
+++ b/packages/jest-circus/src/run.js
@@ -17,7 +17,7 @@ import type {
 
 import {getState, dispatch} from './state';
 import {
-  callAsyncFn,
+  callAsyncCircusFn,
   getAllHooksForDescribe,
   getEachHooksForTest,
   getTestID,
@@ -44,7 +44,7 @@ const _runTestsForDescribeBlock = async (describeBlock: DescribeBlock) => {
   const {beforeAll, afterAll} = getAllHooksForDescribe(describeBlock);
 
   for (const hook of beforeAll) {
-    await _callHook({describeBlock, hook});
+    await _callCircusHook({describeBlock, hook});
   }
 
   // Tests that fail and are retried we run after other tests
@@ -77,7 +77,7 @@ const _runTestsForDescribeBlock = async (describeBlock: DescribeBlock) => {
   }
 
   for (const hook of afterAll) {
-    await _callHook({describeBlock, hook});
+    await _callCircusHook({describeBlock, hook});
   }
   dispatch({describeBlock, name: 'run_describe_finish'});
 };
@@ -105,13 +105,13 @@ const _runTest = async (test: TestEntry): Promise<void> => {
       // hooks after that.
       break;
     }
-    await _callHook({hook, test, testContext});
+    await _callCircusHook({hook, test, testContext});
   }
 
-  await _callTest(test, testContext);
+  await _callCircusTest(test, testContext);
 
   for (const hook of afterEach) {
-    await _callHook({hook, test, testContext});
+    await _callCircusHook({hook, test, testContext});
   }
 
   // `afterAll` hooks should not affect test status (pass or fail), because if
@@ -120,7 +120,7 @@ const _runTest = async (test: TestEntry): Promise<void> => {
   dispatch({name: 'test_done', test});
 };
 
-const _callHook = ({
+const _callCircusHook = ({
   hook,
   test,
   describeBlock,
@@ -133,14 +133,14 @@ const _callHook = ({
 }): Promise<mixed> => {
   dispatch({hook, name: 'hook_start'});
   const timeout = hook.timeout || getState().testTimeout;
-  return callAsyncFn(hook.fn, testContext, {isHook: true, timeout})
+  return callAsyncCircusFn(hook.fn, testContext, {isHook: true, timeout})
     .then(() => dispatch({describeBlock, hook, name: 'hook_success', test}))
     .catch(error =>
       dispatch({describeBlock, error, hook, name: 'hook_failure', test}),
     );
 };
 
-const _callTest = async (
+const _callCircusTest = (
   test: TestEntry,
   testContext: TestContext,
 ): Promise<void> => {
@@ -150,10 +150,10 @@ const _callTest = async (
 
   if (test.errors.length) {
     // We don't run the test if there's already an error in before hooks.
-    return;
+    return Promise.resolve();
   }
 
-  await callAsyncFn(test.fn, testContext, {isHook: false, timeout})
+  return callAsyncCircusFn(test.fn, testContext, {isHook: false, timeout})
     .then(() => dispatch({name: 'test_fn_success', test}))
     .catch(error => dispatch({error, name: 'test_fn_failure', test}));
 };
diff --git a/packages/jest-circus/src/utils.js b/packages/jest-circus/src/utils.js
index 96763d26d345..2f0a44af3c37 100644
--- a/packages/jest-circus/src/utils.js
+++ b/packages/jest-circus/src/utils.js
@@ -164,7 +164,7 @@ const _makeTimeoutMessage = (timeout, isHook) =>
 // the original values in the variables before we require any files.
 const {setTimeout, clearTimeout} = global;
 
-export const callAsyncFn = (
+export const callAsyncCircusFn = (
   fn: AsyncFn,
   testContext: ?TestContext,
   {isHook, timeout}: {isHook?: ?boolean, timeout: number},
diff --git a/packages/jest-cli/src/cli/index.js b/packages/jest-cli/src/cli/index.js
index 13f8af474795..bba73c181171 100644
--- a/packages/jest-cli/src/cli/index.js
+++ b/packages/jest-cli/src/cli/index.js
@@ -110,12 +110,14 @@ export const runCLI = async (
   const {openHandles} = results;
 
   if (openHandles && openHandles.length) {
-    const openHandlesString = pluralize('open handle', openHandles.length, 's');
+    const formatted = formatHandleErrors(openHandles, configs[0]);
+
+    const openHandlesString = pluralize('open handle', formatted.length, 's');
 
     const message =
       chalk.red(
         `\nJest has detected the following ${openHandlesString} potentially keeping Jest from exiting:\n\n`,
-      ) + formatHandleErrors(openHandles, configs[0]).join('\n\n');
+      ) + formatted.join('\n\n');
 
     console.error(message);
   }
diff --git a/packages/jest-cli/src/collectHandles.js b/packages/jest-cli/src/collectHandles.js
index f0fc12144bc2..51e07c502aef 100644
--- a/packages/jest-cli/src/collectHandles.js
+++ b/packages/jest-cli/src/collectHandles.js
@@ -10,6 +10,29 @@
 import type {ProjectConfig} from 'types/Config';
 
 import {formatExecError} from 'jest-message-util';
+import stripAnsi from 'strip-ansi';
+
+function stackIsFromUser(stack) {
+  // Either the test file, or something required by it
+  if (stack.includes('Runtime.requireModule')) {
+    return true;
+  }
+
+  // jest-jasmine it or describe call
+  if (stack.includes('asyncJestTest') || stack.includes('asyncJestLifecycle')) {
+    return true;
+  }
+
+  // An async function call from within circus
+  if (stack.includes('callAsyncCircusFn')) {
+    // jest-circus it or describe call
+    return (
+      stack.includes('_callCircusTest') || stack.includes('_callCircusHook')
+    );
+  }
+
+  return false;
+}
 
 // Inspired by https://github.com/mafintosh/why-is-node-running/blob/master/index.js
 // Extracted as we want to format the result ourselves
@@ -17,7 +40,7 @@ export default function collectHandles(): () => Array<Error> {
   const activeHandles: Map<string, Error> = new Map();
 
   function initHook(asyncId, type) {
-    if (type === 'PROMISE') {
+    if (type === 'PROMISE' || type === 'TIMERWRAP') {
       return;
     }
     const error = new Error(type);
@@ -26,7 +49,7 @@ export default function collectHandles(): () => Array<Error> {
       Error.captureStackTrace(error, initHook);
     }
 
-    if (error.stack.includes('Runtime.requireModule')) {
+    if (stackIsFromUser(error.stack)) {
       activeHandles.set(asyncId, error);
     }
   }
@@ -68,7 +91,33 @@ export function formatHandleErrors(
   errors: Array<Error>,
   config: ProjectConfig,
 ): Array<string> {
-  return errors.map(err =>
-    formatExecError(err, config, {noStackTrace: false}, undefined, true),
+  const stacks = new Set();
+
+  return (
+    errors
+      .map(err =>
+        formatExecError(err, config, {noStackTrace: false}, undefined, true),
+      )
+      // E.g. timeouts might give multiple traces to the same line of code
+      // This hairy filtering tries to remove entries with duplicate stack traces
+      .filter(handle => {
+        const ansiFree: string = stripAnsi(handle);
+
+        const match = ansiFree.match(/\s+at(.*)/);
+
+        if (!match || match.length < 2) {
+          return true;
+        }
+
+        const stack = ansiFree.substr(ansiFree.indexOf(match[1])).trim();
+
+        if (stacks.has(stack)) {
+          return false;
+        }
+
+        stacks.add(stack);
+
+        return true;
+      })
   );
 }
diff --git a/packages/jest-jasmine2/src/jasmine_async.js b/packages/jest-jasmine2/src/jasmine_async.js
index 01b5ec27e87d..d7bb10c481b0 100644
--- a/packages/jest-jasmine2/src/jasmine_async.js
+++ b/packages/jest-jasmine2/src/jasmine_async.js
@@ -39,7 +39,7 @@ function promisifyLifeCycleFunction(originalFn, env) {
 
     // We make *all* functions async and run `done` right away if they
     // didn't return a promise.
-    const asyncFn = function(done) {
+    const asyncJestLifecycle = function(done) {
       const wrappedFn = isGeneratorFn(fn) ? co.wrap(fn) : fn;
       const returnValue = wrappedFn.call({});
 
@@ -57,7 +57,7 @@ function promisifyLifeCycleFunction(originalFn, env) {
       }
     };
 
-    return originalFn.call(env, asyncFn, timeout);
+    return originalFn.call(env, asyncJestLifecycle, timeout);
   };
 }
 
@@ -79,7 +79,7 @@ function promisifyIt(originalFn, env) {
 
     const extraError = new Error();
 
-    const asyncFn = function(done) {
+    const asyncJestTest = function(done) {
       const wrappedFn = isGeneratorFn(fn) ? co.wrap(fn) : fn;
       const returnValue = wrappedFn.call({});
 
@@ -103,7 +103,7 @@ function promisifyIt(originalFn, env) {
       }
     };
 
-    return originalFn.call(env, specName, asyncFn, timeout);
+    return originalFn.call(env, specName, asyncJestTest, timeout);
   };
 }