diff --git a/packages/env/CHANGELOG.md b/packages/env/CHANGELOG.md
index 50943d92016352..bb68681c18f0fd 100644
--- a/packages/env/CHANGELOG.md
+++ b/packages/env/CHANGELOG.md
@@ -2,6 +2,10 @@
 
 ## Unreleased
 
+### Breaking Changes
+
+-   `run` command now has a `--env-cwd` option to set the working directory in the container for the command to execute from.
+
 ## 5.16.0 (2023-04-12)
 
 ## 5.15.0 (2023-03-29)
diff --git a/packages/env/README.md b/packages/env/README.md
index 5c2ac83708a132..7a22dfe88428cf 100644
--- a/packages/env/README.md
+++ b/packages/env/README.md
@@ -316,7 +316,7 @@ The run command can be used to open shell sessions or invoke WP-CLI commands.
 <div class="callout callout-alert">
 In some cases, `wp-env` may consume options that you are attempting to pass to
 the container. This happens with options that `wp-env` has already declared,
-such as `--debug`, `--help`, and `--version`. When this happens, you should fall
+such as `--env-cwd`, `--debug`, `--help`, and `--version`. When this happens, you should fall
 back to using quotation marks; `wp-env` considers everything inside the
 quotation marks to be command argument.
 
@@ -349,6 +349,9 @@ Options:
   --help     Show help                                                 [boolean]
   --version  Show version number                                       [boolean]
   --debug    Enable debug output.                     [boolean] [default: false]
+  --env-cwd  The command's working directory inside of the container. Paths
+             without a leading slash are relative to the WordPress root.
+                                                         [string] [default: "."]
 ```
 
 For example:
diff --git a/packages/env/lib/cli.js b/packages/env/lib/cli.js
index abca20c9b3619a..68316855c6bede 100644
--- a/packages/env/lib/cli.js
+++ b/packages/env/lib/cli.js
@@ -174,6 +174,13 @@ module.exports = function cli() {
 		'run <container> [command..]',
 		'Runs an arbitrary command in one of the underlying Docker containers. The "container" param should reference one of the underlying Docker services like "development", "tests", or "cli". To run a wp-cli command, use the "cli" or "tests-cli" service. You can also use this command to open shell sessions like bash and the WordPress shell in the WordPress instance. For example, `wp-env run cli bash` will open bash in the development WordPress instance. When using long commands with arguments and quotation marks, you need to wrap the "command" param in quotation marks. For example: `wp-env run tests-cli "wp post create --post_type=page --post_title=\'Test\'"` will create a post on the tests WordPress instance.',
 		( args ) => {
+			args.option( 'env-cwd', {
+				type: 'string',
+				requiresArg: true,
+				default: '.',
+				describe:
+					"The command's working directory inside of the container. Paths without a leading slash are relative to the WordPress root.",
+			} );
 			args.positional( 'container', {
 				type: 'string',
 				describe: 'The container to run the command on.',
diff --git a/packages/env/lib/commands/run.js b/packages/env/lib/commands/run.js
index f944d8de84fa53..fd0f800041cb91 100644
--- a/packages/env/lib/commands/run.js
+++ b/packages/env/lib/commands/run.js
@@ -2,6 +2,7 @@
  * External dependencies
  */
 const { spawn } = require( 'child_process' );
+const path = require( 'path' );
 
 /**
  * Internal dependencies
@@ -18,10 +19,17 @@ const initConfig = require( '../init-config' );
  * @param {Object}   options
  * @param {string}   options.container The Docker container to run the command on.
  * @param {string[]} options.command   The command to run.
+ * @param {string}   options.envCwd    The working directory for the command to be executed from.
  * @param {Object}   options.spinner   A CLI spinner which indicates progress.
  * @param {boolean}  options.debug     True if debug mode is enabled.
  */
-module.exports = async function run( { container, command, spinner, debug } ) {
+module.exports = async function run( {
+	container,
+	command,
+	envCwd,
+	spinner,
+	debug,
+} ) {
 	const config = await initConfig( { spinner, debug } );
 
 	command = command.join( ' ' );
@@ -29,12 +37,7 @@ module.exports = async function run( { container, command, spinner, debug } ) {
 	// Shows a contextual tip for the given command.
 	showCommandTips( command, container, spinner );
 
-	await spawnCommandDirectly( {
-		container,
-		command,
-		spinner,
-		config,
-	} );
+	await spawnCommandDirectly( config, container, command, envCwd, spinner );
 
 	spinner.text = `Ran \`${ command }\` in '${ container }'.`;
 };
@@ -42,17 +45,22 @@ module.exports = async function run( { container, command, spinner, debug } ) {
 /**
  * Runs an arbitrary command on the given Docker container.
  *
- * @param {Object}   options
- * @param {string}   options.container The Docker container to run the command on.
- * @param {string}   options.command   The command to run.
- * @param {WPConfig} options.config    The wp-env configuration.
- * @param {Object}   options.spinner   A CLI spinner which indicates progress.
+ * @param {WPConfig} config    The wp-env configuration.
+ * @param {string}   container The Docker container to run the command on.
+ * @param {string}   command   The command to run.
+ * @param {string}   envCwd    The working directory for the command to be executed from.
+ * @param {Object}   spinner   A CLI spinner which indicates progress.
  */
-function spawnCommandDirectly( { container, command, config, spinner } ) {
+function spawnCommandDirectly( config, container, command, envCwd, spinner ) {
+	// We need to pass absolute paths to the container.
+	envCwd = path.resolve( '/var/www/html', envCwd );
+
 	const composeCommand = [
 		'-f',
 		config.dockerComposeConfigPath,
 		'run',
+		'-w',
+		envCwd,
 		'--rm',
 		container,
 		...command.split( ' ' ), // The command will fail if passed as a complete string.