diff --git a/tools/cli/cliRouter.js b/tools/cli/cliRouter.js
index ed19849cb6ae..1ce398ed010a 100644
--- a/tools/cli/cliRouter.js
+++ b/tools/cli/cliRouter.js
@@ -13,6 +13,7 @@ import { generateDefine } from './commands/generate.js';
 import * as installCommand from './commands/install.js';
 import * as noopCommand from './commands/noop.js';
 import * as phanCommand from './commands/phan.js';
+import * as playgroundCommand from './commands/playground.js';
 import * as pnpmCommand from './commands/pnpm.js';
 import { releaseDefine } from './commands/release.js';
 import { rsyncDefine } from './commands/rsync.js';
@@ -49,6 +50,7 @@ export async function cli() {
 	argv.command( installCommand );
 	argv.command( noopCommand );
 	argv.command( phanCommand );
+	argv.command( playgroundCommand );
 	argv.command( pnpmCommand );
 	argv = releaseDefine( argv );
 	argv = rsyncDefine( argv );
diff --git a/tools/cli/commands/playground.js b/tools/cli/commands/playground.js
new file mode 100644
index 000000000000..bb0c5b1d0b93
--- /dev/null
+++ b/tools/cli/commands/playground.js
@@ -0,0 +1,301 @@
+import child_process from 'child_process';
+import fs from 'fs';
+import os from 'os';
+import path from 'path';
+import { fileURLToPath } from 'url';
+import chalk from 'chalk';
+import { projectDir } from '../helpers/install.js';
+import { maybePromptForPlugin } from './rsync.js';
+
+const cliPath = fileURLToPath( new URL( '../bin/jetpack.js', import.meta.url ) );
+
+export const command = 'playground [plugin]';
+export const describe = 'Starts a WordPress Playground instance with a plugin mounted';
+
+/**
+ * Options definition for the playground subcommand.
+ *
+ * @param {object} yargs - The Yargs dependency.
+ * @return {object} Yargs with the playground commands defined.
+ */
+export function builder( yargs ) {
+	return yargs
+		.positional( 'plugin', {
+			describe: 'Plugin name, e.g. jetpack',
+			type: 'string',
+		} )
+		.option( 'blueprint', {
+			alias: 'b',
+			type: 'string',
+			description: 'Path to a custom blueprint.json file',
+		} )
+		.option( 'port', {
+			alias: 'p',
+			type: 'number',
+			description: 'Port to run the Playground server on',
+		} )
+		.example( 'jetpack playground jetpack', 'Start Playground with the Jetpack plugin' )
+		.example( 'jetpack playground crm', 'Start Playground with the CRM plugin' );
+}
+
+/**
+ * Entry point for the playground CLI.
+ *
+ * @param {object} argv - The argv for the command line.
+ */
+export async function handler( argv ) {
+	argv = await maybePromptForPlugin( argv );
+
+	// Validate port if provided.
+	if ( argv.port !== undefined ) {
+		if ( ! Number.isInteger( argv.port ) || argv.port < 1 || argv.port > 65535 ) {
+			console.error( chalk.red( 'Port must be an integer between 1 and 65535.' ) );
+			process.exit( 1 );
+		}
+	}
+
+	// Warn if @wp-playground/cli needs to be downloaded (first run).
+	const playgroundCheck = child_process.spawnSync(
+		'npx',
+		[ '--no-install', '@wp-playground/cli', '--version' ],
+		{ stdio: 'ignore' }
+	);
+	if ( playgroundCheck.status !== 0 ) {
+		console.log(
+			chalk.yellow(
+				'@wp-playground/cli is not yet cached. The first run will download it, which may take a moment.'
+			)
+		);
+	}
+
+	const pluginPath = projectDir( `plugins/${ argv.plugin }` );
+
+	// Read the plugin slug from composer.json so the mount path inside
+	// Playground uses the correct wp-plugin-slug (e.g. zero-bs-crm for crm).
+	const composerJsonPath = path.join( pluginPath, 'composer.json' );
+	let wpPluginSlug = argv.plugin;
+	if ( fs.existsSync( composerJsonPath ) ) {
+		try {
+			const composerJson = JSON.parse( fs.readFileSync( composerJsonPath, 'utf8' ) );
+			wpPluginSlug =
+				composerJson?.extra?.[ 'wp-plugin-slug' ] ??
+				composerJson?.extra?.[ 'beta-plugin-slug' ] ??
+				argv.plugin;
+		} catch {
+			// Fall back to directory name if composer.json is unreadable.
+		}
+	}
+
+	// If the plugin hasn't been built, run the build first.
+	if (
+		! fs.existsSync( path.join( pluginPath, 'vendor' ) ) ||
+		! fs.existsSync( path.join( pluginPath, 'node_modules' ) )
+	) {
+		console.log(
+			chalk.yellow( `Plugin "${ argv.plugin }" does not appear to be built. Building...` )
+		);
+		const build = child_process.spawnSync(
+			process.execPath,
+			[ cliPath, 'build', `plugins/${ argv.plugin }` ],
+			{ stdio: 'inherit' }
+		);
+		if ( build.status !== 0 ) {
+			console.error(
+				chalk.red( 'Build failed. Please run "jetpack build" manually and try again.' )
+			);
+			process.exit( 1 );
+		}
+	}
+
+	// Build the blueprint into a temp directory.
+	const tmpDir = fs.mkdtempSync( path.join( os.tmpdir(), `jetpack-playground-${ argv.plugin }-` ) );
+
+	// The vendor/jetpack_vendor directories contain symlinks like
+	// ../../../../packages/<name>/ which, from the plugin location at
+	// /wordpress/wp-content/plugins/<slug>/jetpack_vendor/automattic/<pkg>,
+	// resolve to /wordpress/wp-content/packages/<name>/. We mount
+	// projects/packages there so these symlinks resolve to real files and
+	// plugins_url() can generate correct URLs (paths stay under wp-content).
+	const packagesPath = projectDir( 'packages' );
+
+	try {
+		const blueprintPath = buildBlueprint( pluginPath, tmpDir, argv, wpPluginSlug );
+
+		const port = argv.port ?? 9400;
+
+		const args = [
+			'@wp-playground/cli',
+			'server',
+			`--mount=${ pluginPath }:/wordpress/wp-content/plugins/${ wpPluginSlug }`,
+			`--mount=${ packagesPath }:/wordpress/wp-content/packages`,
+			`--blueprint=${ blueprintPath }`,
+		];
+
+		if ( argv.port !== undefined ) {
+			args.push( `--port=${ argv.port }` );
+		}
+
+		if ( argv.verbose ) {
+			console.log( chalk.gray( `Running: npx ${ args.join( ' ' ) }` ) );
+		}
+
+		await new Promise( ( resolve, reject ) => {
+			const proc = child_process.spawn( 'npx', args, {
+				stdio: [ 'inherit', 'pipe', 'inherit' ],
+			} );
+
+			proc.stdout.on( 'data', data => {
+				process.stdout.write( data );
+
+				// After Playground prints its "Ready!" line, show helpful info.
+				if ( data.toString().includes( 'Ready!' ) ) {
+					console.log();
+					console.log( `  Admin:  ${ chalk.cyan( `http://127.0.0.1:${ port }/wp-admin/` ) }` );
+					console.log( chalk.gray( '  Login:  admin / password' ) );
+					console.log( chalk.gray( '  Stop:   Ctrl+C' ) );
+					console.log();
+				}
+			} );
+
+			proc.on( 'close', code => {
+				if ( code !== 0 && code !== null ) {
+					reject( new Error( `Playground exited with code ${ code }` ) );
+				} else {
+					resolve();
+				}
+			} );
+
+			proc.on( 'error', reject );
+		} );
+	} finally {
+		console.log( chalk.gray( 'Cleaning up temporary files...' ) );
+		fs.rmSync( tmpDir, { recursive: true, force: true } );
+	}
+}
+
+/**
+ * Build a blueprint JSON file for the Playground session.
+ *
+ * Always injects a step to define JETPACK_DEV_DEBUG in wp-config.php so Jetpack
+ * runs in offline mode without needing a WordPress.com connection. If the plugin
+ * ships its own blueprint, the steps are merged.
+ *
+ * @param {string} pluginPath   - Absolute path to the plugin source directory.
+ * @param {string} tmpDir       - Temporary directory to write the blueprint into.
+ * @param {object} options      - CLI options (may include a custom blueprint path and plugin name).
+ * @param {string} wpPluginSlug - The WordPress plugin slug (used for activation).
+ * @return {string} Path to the generated blueprint file.
+ */
+function buildBlueprint( pluginPath, tmpDir, options, wpPluginSlug ) {
+	// Start with a base blueprint.
+	let blueprint = {
+		$schema: 'https://playground.wordpress.net/blueprint-schema.json',
+		landingPage: '/wp-admin/',
+		login: true,
+		features: {
+			networking: true,
+		},
+		steps: [],
+	};
+
+	// Merge a user-provided or plugin-shipped blueprint.
+	let sourceBlueprint = null;
+	if ( options.blueprint ) {
+		sourceBlueprint = path.resolve( options.blueprint );
+		if ( ! fs.existsSync( sourceBlueprint ) ) {
+			console.error( chalk.red( `Blueprint file not found: ${ sourceBlueprint }` ) );
+			process.exit( 1 );
+		}
+	} else {
+		const pluginBlueprintPath = path.join(
+			pluginPath,
+			'.wordpress-org',
+			'blueprints',
+			'blueprint.json'
+		);
+		if ( fs.existsSync( pluginBlueprintPath ) ) {
+			sourceBlueprint = pluginBlueprintPath;
+		}
+	}
+
+	if ( sourceBlueprint ) {
+		console.log( chalk.gray( `Using blueprint: ${ path.relative( '.', sourceBlueprint ) }` ) );
+		let custom;
+		try {
+			custom = JSON.parse( fs.readFileSync( sourceBlueprint, 'utf8' ) );
+		} catch ( err ) {
+			console.error( chalk.red( `Failed to parse blueprint: ${ err.message }` ) );
+			process.exit( 1 );
+		}
+		blueprint = {
+			...blueprint,
+			...custom,
+			// Merge steps — custom steps run first, then ours.
+			steps: [ ...( custom.steps || [] ), ...blueprint.steps ],
+		};
+	}
+
+	// The vendor symlinks resolve to /wordpress/wp-content/packages/ which is
+	// outside WP_PLUGIN_DIR, so plugins_url() generates broken URLs like
+	// /wp-content/plugins/wordpress/wp-content/packages/... Install a mu-plugin
+	// that rewrites these URLs to the correct /wp-content/packages/ path.
+	blueprint.steps.push( {
+		step: 'writeFile',
+		path: '/wordpress/wp-content/mu-plugins/playground-fix-symlinks.php',
+		data: `<?php
+/**
+ * Fix plugins_url() for monorepo vendor symlinks in Playground.
+ *
+ * Vendor symlinks resolve outside WP_PLUGIN_DIR to /wordpress/wp-content/packages/.
+ * This filter rewrites the broken URLs so the assets load correctly.
+ */
+add_filter( 'plugins_url', function ( $url ) {
+	return str_replace( '/wp-content/plugins/wordpress/wp-content/packages/', '/wp-content/packages/', $url );
+} );
+`,
+	} );
+
+	// Inject the offline mode step: define JETPACK_DEV_DEBUG in wp-config.php.
+	blueprint.steps.push( {
+		step: 'defineWpConfigConsts',
+		consts: {
+			JETPACK_DEV_DEBUG: true,
+		},
+	} );
+
+	// Activate the plugin using the WordPress plugin identifier (slug/main-file.php).
+	const mainFile = findMainPluginFile( pluginPath );
+	if ( mainFile ) {
+		blueprint.steps.push( {
+			step: 'activatePlugin',
+			pluginPath: `${ wpPluginSlug }/${ mainFile }`,
+		} );
+	}
+
+	// Write the merged blueprint to the temp directory.
+	const blueprintOutPath = path.join( tmpDir, 'blueprint.json' );
+	fs.writeFileSync( blueprintOutPath, JSON.stringify( blueprint, null, '\t' ) );
+
+	return blueprintOutPath;
+}
+
+/**
+ * Find the main plugin PHP file by looking for the "Plugin Name:" header
+ * in root-level PHP files.
+ *
+ * @param {string} pluginPath - Absolute path to the plugin directory.
+ * @return {string|null} The filename of the main plugin file, or null if not found.
+ */
+function findMainPluginFile( pluginPath ) {
+	const entries = fs.readdirSync( pluginPath, { withFileTypes: true } );
+	for ( const entry of entries ) {
+		if ( ! entry.isFile() || ! entry.name.endsWith( '.php' ) ) {
+			continue;
+		}
+		const content = fs.readFileSync( path.join( pluginPath, entry.name ), 'utf8' );
+		if ( /^\s*\*?\s*Plugin Name:/m.test( content ) ) {
+			return entry.name;
+		}
+	}
+	return null;
+}