diff --git a/packages/env/lib/create-docker-compose-config.js b/packages/env/lib/create-docker-compose-config.js
index f5971723148b57..84ab2490828aa0 100644
--- a/packages/env/lib/create-docker-compose-config.js
+++ b/packages/env/lib/create-docker-compose-config.js
@@ -1,11 +1,15 @@
 module.exports = function createDockerComposeConfig(
-	cwd,
-	cwdName,
 	cwdTestsPath,
-	context
+	context,
+	dependencies,
 ) {
+	const { path: cwd, pathBasename: cwdName } = context;
+
+	const dependencyMappings = [ ...dependencies, context ].map(
+		( { path, pathBasename, type } ) => `      - ${ path }/:/var/www/html/wp-content/${ type }s/${ pathBasename }/\n`
+	).join( '' );
 	const commonVolumes = `
-      - ${ cwd }/:/var/www/html/wp-content/${ context.type }s/${ cwdName }/
+${ dependencyMappings }
       - ${ cwd }${ cwdTestsPath }/e2e-tests/mu-plugins/:/var/www/html/wp-content/mu-plugins/
       - ${ cwd }${ cwdTestsPath }/e2e-tests/plugins/:/var/www/html/wp-content/plugins/${ cwdName }-test-plugins/`;
 	const volumes = `
diff --git a/packages/env/lib/detect-context.js b/packages/env/lib/detect-context.js
index afc23f6dd5f6f3..8e1f9551b659d3 100644
--- a/packages/env/lib/detect-context.js
+++ b/packages/env/lib/detect-context.js
@@ -13,14 +13,34 @@ const path = require( 'path' );
 const readDir = util.promisify( fs.readdir );
 const finished = util.promisify( stream.finished );
 
-module.exports = async function detectContext() {
+/**
+ * @typedef Context
+ * @type {Object}
+ * @property {string} type
+ * @property {string} path
+ * @property {string} pathBasename
+ */
+
+/**
+ * Detects the context of a given path.
+ *
+ * @param {string} [directoryPath=process.cwd()] The directory to detect. Should point to a directory, defaulting to the current working directory.
+ *
+ * @return {Context} The context of the directory. If a theme or plugin, the type property will contain 'theme' or 'plugin'.
+ */
+module.exports = async function detectContext( directoryPath = process.cwd() ) {
 	const context = {};
 
+	// Use absolute paths to files so that we can properly read
+	// dependencies not in the current working directory.
+	const absPath = path.resolve( directoryPath );
+
 	// Race multiple file read streams against each other until
 	// a plugin or theme header is found.
-	const files = ( await readDir( './' ) ).filter(
+	const files = ( await readDir( absPath ) ).filter(
 		( file ) => path.extname( file ) === '.php' || path.basename( file ) === 'style.css'
-	);
+	).map( ( fileName ) => path.join( absPath, fileName ) );
+
 	const streams = [];
 	for ( const file of files ) {
 		const fileStream = fs.createReadStream( file, 'utf8' );
@@ -28,6 +48,8 @@ module.exports = async function detectContext() {
 			const [ , type ] = text.match( /(Plugin|Theme) Name: .*[\r\n]/ ) || [];
 			if ( type ) {
 				context.type = type.toLowerCase();
+				context.path = absPath;
+				context.pathBasename = path.basename( absPath );
 
 				// Stop the creation of new streams by mutating the iterated array. We can't `break`, because we are inside a function.
 				files.splice( 0 );
diff --git a/packages/env/lib/env.js b/packages/env/lib/env.js
index c2ba83ac24c221..232fba9910cdf6 100644
--- a/packages/env/lib/env.js
+++ b/packages/env/lib/env.js
@@ -11,8 +11,9 @@ const wait = require( 'util' ).promisify( setTimeout );
 /**
  * Internal dependencies
  */
-const detectContext = require( './detect-context' );
 const createDockerComposeConfig = require( './create-docker-compose-config' );
+const detectContext = require( './detect-context' );
+const resolveDependencies = require( './resolve-dependencies' );
 
 // Config Variables
 const cwd = process.cwd();
@@ -38,14 +39,15 @@ const setupSite = ( isTests = false ) =>
 		} --title=${ cwdName } --admin_user=admin --admin_password=password --admin_email=admin@wordpress.org`,
 		isTests
 	);
-const activateContext = ( context, isTests = false ) =>
-	wpCliRun( `wp ${ context.type } activate ${ cwdName }`, isTests );
+const activateContext = ( { type, pathBasename }, isTests = false ) =>
+	wpCliRun( `wp ${ type } activate ${ pathBasename }`, isTests );
 const resetDatabase = ( isTests = false ) =>
 	wpCliRun( 'wp db reset --yes', isTests );
 
 module.exports = {
 	async start( { ref, spinner = {} } ) {
 		const context = await detectContext();
+		const dependencies = await resolveDependencies();
 
 		spinner.text = `Downloading WordPress@${ ref } 0/100%.`;
 		const gitFetchOptions = {
@@ -100,7 +102,7 @@ module.exports = {
 		spinner.text = `Starting WordPress@${ ref }.`;
 		fs.writeFileSync(
 			dockerComposeOptions.config,
-			createDockerComposeConfig( cwd, cwdName, cwdTestsPath, context )
+			createDockerComposeConfig( cwdTestsPath, context, dependencies )
 		);
 
 		// These will bring up the database container,
@@ -127,6 +129,7 @@ module.exports = {
 		await Promise.all( [
 			activateContext( context ),
 			activateContext( context, true ),
+			...dependencies.map( activateContext ),
 		] );
 
 		// Remove dangling containers and finish.
@@ -142,6 +145,8 @@ module.exports = {
 
 	async clean( { environment, spinner } ) {
 		const context = await detectContext();
+		const dependencies = await resolveDependencies();
+		const activateDependencies = () => Promise.all( dependencies.map( activateContext ) );
 
 		const description = `${ environment } environment${
 			environment === 'all' ? 's' : ''
@@ -155,6 +160,7 @@ module.exports = {
 				resetDatabase()
 					.then( setupSite )
 					.then( activateContext.bind( null, context ) )
+					.then( activateDependencies )
 					.catch( () => {} )
 			);
 		}
diff --git a/packages/env/lib/resolve-dependencies.js b/packages/env/lib/resolve-dependencies.js
new file mode 100644
index 00000000000000..4ff1205acd8d50
--- /dev/null
+++ b/packages/env/lib/resolve-dependencies.js
@@ -0,0 +1,44 @@
+'use strict';
+
+/**
+ * External dependencies
+ */
+const util = require( 'util' );
+const fs = require( 'fs' );
+
+/**
+ * Internal dependencies
+ */
+const detectContext = require( './detect-context' );
+
+/**
+ * Promisified dependencies
+ */
+const readFile = util.promisify( fs.readFile );
+
+/**
+ * Returns an array of dependencies to be mounted in the Docker image.
+ *
+ * Reads from the wp-env.json file in the current directory and uses detect
+ * context to make sure the specified dependencies exist and are plugins
+ * and/or themes.
+ *
+ * @return {Array<detectContext.Context>} An array of dependencies in the context format.
+ */
+module.exports = async function resolveDependencies() {
+	const envFile = await readFile( './wp-env.json' );
+	const { themes, plugins } = JSON.parse( envFile );
+
+	const dependencyResolvers = [];
+	if ( Array.isArray( themes ) ) {
+		dependencyResolvers.push( ...themes.map( detectContext ) );
+	}
+
+	if ( Array.isArray( plugins ) ) {
+		dependencyResolvers.push( ...plugins.map( detectContext ) );
+	}
+
+	// Return all dependencies which have been detected to be a plugin or a theme.
+	const dependencies = await Promise.all( dependencyResolvers );
+	return dependencies.filter( ( { type } ) => !! type );
+};