diff --git a/CHANGELOG.md b/CHANGELOG.md
index 5c02eb4c007f..5aef0e7173e2 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -50,6 +50,7 @@
 - `[jest-circus]` Fix `testLocation` on Windows when using `test.each` ([#10871](https://github.com/facebook/jest/pull/10871))
 - `[jest-cli]` Use testFailureExitCode when bailing from a failed test ([#10958](https://github.com/facebook/jest/pull/10958))
 - `[jest-cli]` Print custom error if error thrown from global hooks is not an error already ([#11003](https://github.com/facebook/jest/pull/11003))
+- `[jest-cli]` Allow running multiple "projects" from programmatic API ([#11307](https://github.com/facebook/jest/pull/11307))
 - `[jest-config]` [**BREAKING**] Change default file extension order by moving json behind ts and tsx ([10572](https://github.com/facebook/jest/pull/10572))
 - `[jest-console]` `console.dir` now respects the second argument correctly ([#10638](https://github.com/facebook/jest/pull/10638))
 - `[jest-core]` Don't report PerformanceObserver as open handle ([#11123](https://github.com/facebook/jest/pull/11123))
diff --git a/e2e/__tests__/__snapshots__/runProgrammaticallyMultipleProjects.test.ts.snap b/e2e/__tests__/__snapshots__/runProgrammaticallyMultipleProjects.test.ts.snap
new file mode 100644
index 000000000000..3362f97f2234
--- /dev/null
+++ b/e2e/__tests__/__snapshots__/runProgrammaticallyMultipleProjects.test.ts.snap
@@ -0,0 +1,9 @@
+// Jest Snapshot v1, https://goo.gl/fbAQLP
+
+exports[`run programmatically with multiple projects: summary 1`] = `
+Test Suites: 2 passed, 2 total
+Tests:       2 passed, 2 total
+Snapshots:   0 total
+Time:        <<REPLACED>>
+Ran all test suites in 2 projects.
+`;
diff --git a/e2e/__tests__/runProgrammaticallyMultipleProjects.test.ts b/e2e/__tests__/runProgrammaticallyMultipleProjects.test.ts
new file mode 100644
index 000000000000..16b3c257949f
--- /dev/null
+++ b/e2e/__tests__/runProgrammaticallyMultipleProjects.test.ts
@@ -0,0 +1,20 @@
+/**
+ * Copyright (c) Facebook, Inc. and its affiliates. All Rights Reserved.
+ *
+ * This source code is licensed under the MIT license found in the
+ * LICENSE file in the root directory of this source tree.
+ */
+
+import {resolve} from 'path';
+import {wrap} from 'jest-snapshot-serializer-raw';
+import stripAnsi = require('strip-ansi');
+import {extractSummary, run} from '../Utils';
+
+const dir = resolve(__dirname, '../run-programmatically-multiple-projects');
+
+test('run programmatically with multiple projects', () => {
+  const {stderr, exitCode} = run(`node run-jest.js`, dir);
+  const {summary} = extractSummary(stripAnsi(stderr));
+  expect(exitCode).toEqual(0);
+  expect(wrap(summary)).toMatchSnapshot('summary');
+});
diff --git a/e2e/run-programmatically-multiple-projects/client/client.test.js b/e2e/run-programmatically-multiple-projects/client/client.test.js
new file mode 100644
index 000000000000..c40068258659
--- /dev/null
+++ b/e2e/run-programmatically-multiple-projects/client/client.test.js
@@ -0,0 +1,10 @@
+/**
+ * Copyright (c) Facebook, Inc. and its affiliates. All Rights Reserved.
+ *
+ * This source code is licensed under the MIT license found in the
+ * LICENSE file in the root directory of this source tree.
+ */
+
+describe('client', () => {
+  it('should work', () => {});
+});
diff --git a/e2e/run-programmatically-multiple-projects/package.json b/e2e/run-programmatically-multiple-projects/package.json
new file mode 100644
index 000000000000..142909ad236a
--- /dev/null
+++ b/e2e/run-programmatically-multiple-projects/package.json
@@ -0,0 +1,6 @@
+{
+  "name": "runcli-multiple-projects",
+  "version": "1.0.0",
+  "dependencies": {},
+  "jest": {}
+}
diff --git a/e2e/run-programmatically-multiple-projects/run-jest.js b/e2e/run-programmatically-multiple-projects/run-jest.js
new file mode 100644
index 000000000000..06d66e72f007
--- /dev/null
+++ b/e2e/run-programmatically-multiple-projects/run-jest.js
@@ -0,0 +1,22 @@
+/**
+ * Copyright (c) Facebook, Inc. and its affiliates. All Rights Reserved.
+ *
+ * This source code is licensed under the MIT license found in the
+ * LICENSE file in the root directory of this source tree.
+ */
+
+const {runCLI} = require('@jest/core');
+
+const config = {
+  projects: [
+    {testMatch: ['<rootDir>/client/**/*.test.js']},
+    {testMatch: ['<rootDir>/server/**/*.test.js']},
+  ],
+};
+
+runCLI({config: JSON.stringify(config)}, [process.cwd()])
+  .then(() => console.log('run-programmatically-mutiple-projects completed'))
+  .catch(err => {
+    console.error(err);
+    process.exitCode = 1;
+  });
diff --git a/e2e/run-programmatically-multiple-projects/server/server.test.js b/e2e/run-programmatically-multiple-projects/server/server.test.js
new file mode 100644
index 000000000000..96820356c380
--- /dev/null
+++ b/e2e/run-programmatically-multiple-projects/server/server.test.js
@@ -0,0 +1,10 @@
+/**
+ * Copyright (c) Facebook, Inc. and its affiliates. All Rights Reserved.
+ *
+ * This source code is licensed under the MIT license found in the
+ * LICENSE file in the root directory of this source tree.
+ */
+
+describe('server', () => {
+  it('should work', () => {});
+});
diff --git a/packages/jest-config/src/index.ts b/packages/jest-config/src/index.ts
index 490cc769000d..35bc4f524e85 100644
--- a/packages/jest-config/src/index.ts
+++ b/packages/jest-config/src/index.ts
@@ -38,7 +38,7 @@ export async function readConfig(
   // `project` property, we don't want to read `--config` value and rather
   // read individual configs for every project.
   skipArgvConfigOption?: boolean,
-  parentConfigPath?: Config.Path | null,
+  parentConfigDirname?: Config.Path | null,
   projectIndex: number = Infinity,
 ): Promise<ReadConfig> {
   let rawOptions:
@@ -47,8 +47,7 @@ export async function readConfig(
   let configPath = null;
 
   if (typeof packageRootOrConfig !== 'string') {
-    if (parentConfigPath) {
-      const parentConfigDirname = path.dirname(parentConfigPath);
+    if (parentConfigDirname) {
       rawOptions = packageRootOrConfig;
       rawOptions.rootDir = rawOptions.rootDir
         ? replaceRootDirInPath(parentConfigDirname, rawOptions.rootDir)
@@ -301,10 +300,9 @@ export async function readConfigs(
   }
 
   if (projects.length > 0) {
-    const projectIsCwd =
-      process.platform === 'win32'
-        ? projects[0] === tryRealpath(process.cwd())
-        : projects[0] === process.cwd();
+    const cwd =
+      process.platform === 'win32' ? tryRealpath(process.cwd()) : process.cwd();
+    const projectIsCwd = projects[0] === cwd;
 
     const parsedConfigs = await Promise.all(
       projects
@@ -332,7 +330,7 @@ export async function readConfigs(
             argv,
             root,
             skipArgvConfigOption,
-            configPath,
+            configPath ? path.dirname(configPath) : cwd,
             projectIndex,
           );
         }),