diff --git a/src/wp-admin/css/customize-controls.css b/src/wp-admin/css/customize-controls.css
index 3234eb6249..adbd862be8 100644
--- a/src/wp-admin/css/customize-controls.css
+++ b/src/wp-admin/css/customize-controls.css
@@ -565,8 +565,8 @@ p.customize-section-description {
 }
 
 .customize-control select {
-	min-width: 50%;
-	max-width: 100%;
+	width: 100%;
+	max-width: 300px;
 	height: 28px;
 	line-height: 28px;
 }
@@ -587,6 +587,7 @@ p.customize-section-description {
 	display: block;
 	font-style: italic;
 	line-height: 18px;
+	margin-top: 0;
 	margin-bottom: 5px;
 }
 
@@ -674,6 +675,54 @@ p.customize-section-description {
 	float: left;
 }
 
+#available-menu-items .accordion-section-content .new-content-item,
+.customize-control-dropdown-pages .new-content-item {
+	width: -webkit-calc(100% - 30px);
+	width: calc(100% - 30px);
+	padding: 8px 15px;
+	position: absolute;
+	bottom: 0;
+	z-index: 10;
+	background: #eee;
+	display: -webkit-box;
+	display: -moz-box;
+	display: -ms-flexbox;
+	display: -webkit-flex;
+	display: flex;
+}
+
+.customize-control-dropdown-pages .new-content-item {
+	width: 100%;
+	max-width: 300px;
+	padding: 5px 0 5px 1px;
+	position: relative;
+}
+
+#available-menu-items .new-content-item .create-item-input,
+.customize-control-dropdown-pages .new-content-item .create-item-input {
+	-webkit-box-flex: 10;
+	-webkit-flex-grow: 10;
+	-moz-box-flex: 10;
+	-ms-flex-positive: 10;
+	-ms-flex: 10;
+	flex-grow: 10;
+}
+
+#available-menu-items .new-content-item .add-content,
+.customize-control-dropdown-pages .new-content-item .add-content {
+	margin: 2px 0 2px 6px;
+	-webkit-box-flex: 10;
+	-webkit-flex-grow: 10;
+	-moz-box-flex: 10;
+	-ms-flex-positive: 10;
+	-ms-flex: 10;
+	flex-grow: 1;
+}
+
+.customize-control-dropdown-pages .new-content-item .create-item-input.invalid {
+	border: 1px solid #f00;
+}
+
 #customize-preview iframe {
 	width: 100%;
 	height: 100%;
diff --git a/src/wp-admin/css/customize-nav-menus.css b/src/wp-admin/css/customize-nav-menus.css
index 1386fe0940..a63df15975 100644
--- a/src/wp-admin/css/customize-nav-menus.css
+++ b/src/wp-admin/css/customize-nav-menus.css
@@ -572,41 +572,6 @@
 	padding: 0 15px 15px 15px;
 }
 
-#available-menu-items .accordion-section-content .new-content-item {
-	width: -webkit-calc(100% - 30px);
-	width: calc(100% - 30px);
-	padding: 8px 15px;
-	position: absolute;
-	bottom: 0;
-	z-index: 10;
-	background: #eee;
-	display: -webkit-box;
-	display: -moz-box;
-	display: -ms-flexbox;
-	display: -webkit-flex;
-	display: flex;
-}
-
-#available-menu-items .new-content-item .create-item-input {
-	-webkit-box-flex: 10;
-	-webkit-flex-grow: 10;
-	-moz-box-flex: 10;
-	-ms-flex-positive: 10;
-	-ms-flex: 10;
-	flex-grow: 10;
-	margin-left: 5px;
-	padding: 4.5px;
-}
-#available-menu-items .new-content-item .add-content {
-	padding-left: 6px;
-	-webkit-box-flex: 10;
-	-webkit-flex-grow: 10;
-	-moz-box-flex: 10;
-	-ms-flex-positive: 10;
-	-ms-flex: 10;
-	flex-grow: 1;
-}
-
 #available-menu-items .menu-item-tpl {
 	margin: 0;
 }
diff --git a/src/wp-admin/js/customize-controls.js b/src/wp-admin/js/customize-controls.js
index a23a130c0b..90b8411fb6 100644
--- a/src/wp-admin/js/customize-controls.js
+++ b/src/wp-admin/js/customize-controls.js
@@ -2516,9 +2516,28 @@
 		/**
 		 * Triggered when the control's markup has been injected into the DOM.
 		 *
-		 * @abstract
+		 * @returns {void}
 		 */
-		ready: function() {},
+		ready: function() {
+			var control = this, newItem;
+			if ( 'dropdown-pages' === control.params.type && control.params.allow_addition ) {
+				newItem = control.container.find( '.new-content-item' );
+				newItem.hide(); // Hide in JS to preserve flex display when showing.
+				control.container.on( 'click', '.add-new-toggle', function( e ) {
+					$( e.currentTarget ).slideUp( 180 );
+					newItem.slideDown( 180 );
+					newItem.find( '.create-item-input' ).focus();
+				});
+				control.container.on( 'click', '.add-content', function() {
+					control.addNewPage();
+				});
+				control.container.on( 'keyup', '.create-item-input', function( e ) {
+					if ( 13 === e.which ) { // Enter
+						control.addNewPage();
+					}
+				});
+			}
+		},
 
 		/**
 		 * Get the element inside of a control's container that contains the validation error message.
@@ -2736,6 +2755,73 @@
 					control.container.html( template( control.params ) );
 				}
 			}
+		},
+
+		/**
+		 * Add a new page to a dropdown-pages control reusing menus code for this.
+		 *
+		 * @since 4.7.0
+		 * @access private
+		 * @returns {void}
+		 */
+		addNewPage: function () {
+			var control = this, promise, toggle, container, input, title, select;
+
+			if ( 'dropdown-pages' !== control.params.type || ! control.params.allow_addition || ! api.Menus ) {
+				return;
+			}
+
+			toggle = control.container.find( '.add-new-toggle' );
+			container = control.container.find( '.new-content-item' );
+			input = control.container.find( '.create-item-input' );
+			title = input.val();
+			select = control.container.find( 'select' );
+
+			if ( ! title ) {
+				input.addClass( 'invalid' );
+				return;
+			}
+
+			input.removeClass( 'invalid' );
+			input.attr( 'disabled', 'disabled' );
+
+			// The menus functions add the page, publish when appropriate, and also add the new page to the dropdown-pages controls.
+			promise = api.Menus.insertAutoDraftPost( {
+				post_title: title,
+				post_type: 'page'
+			} );
+			promise.done( function( data ) {
+				var availableItem, $content, itemTemplate;
+
+				// Prepare the new page as an available menu item.
+				// See api.Menus.submitNew().
+				availableItem = new api.Menus.AvailableItemModel( {
+					'id': 'post-' + data.post_id, // Used for available menu item Backbone models.
+					'title': title,
+					'type': 'page',
+					'type_label': api.Menus.data.l10n.page_label,
+					'object': 'post_type',
+					'object_id': data.post_id,
+					'url': data.url
+				} );
+
+				// Add the new item to the list of available menu items.
+				api.Menus.availableMenuItemsPanel.collection.add( availableItem );
+				$content = $( '#available-menu-items-post_type-page' ).find( '.available-menu-items-list' );
+				itemTemplate = wp.template( 'available-menu-item' );
+				$content.prepend( itemTemplate( availableItem.attributes ) );
+
+				// Focus the select control.
+				select.focus();
+				control.setting.set( String( data.post_id ) ); // Triggers a preview refresh and updates the setting.
+
+				// Reset the create page form.
+				container.slideUp( 180 );
+				toggle.slideDown( 180 );
+			} )
+			.always( function() {
+				input.val( '' ).removeAttr( 'disabled' );
+			} );
 		}
 	});
 
diff --git a/src/wp-admin/js/customize-nav-menus.js b/src/wp-admin/js/customize-nav-menus.js
index 9981cc92ef..6024739059 100644
--- a/src/wp-admin/js/customize-nav-menus.js
+++ b/src/wp-admin/js/customize-nav-menus.js
@@ -101,7 +101,6 @@
 
 		request.done( function( response ) {
 			if ( response.post_id ) {
-				deferred.resolve( response );
 				api.Menus.insertedAutoDrafts.push( response.post_id );
 				api( 'nav_menus_created_posts' ).set( _.clone( api.Menus.insertedAutoDrafts ) );
 
@@ -121,6 +120,7 @@
 						}
 					} );
 				}
+				deferred.resolve( response );
 			}
 		} );
 
diff --git a/src/wp-includes/class-wp-customize-control.php b/src/wp-includes/class-wp-customize-control.php
index e8482b2df0..c45af67d8f 100644
--- a/src/wp-includes/class-wp-customize-control.php
+++ b/src/wp-includes/class-wp-customize-control.php
@@ -114,6 +114,15 @@ class WP_Customize_Control {
 	 */
 	public $input_attrs = array();
 
+	/**
+	 * Show UI for adding new content, currently only used for the dropdown-pages control.
+	 *
+	 * @since 4.7.0
+	 * @access public
+	 * @var array
+	 */
+	public $allow_addition = false;
+
 	/**
 	 * @deprecated It is better to just call the json() method
 	 * @access public
@@ -296,6 +305,10 @@ class WP_Customize_Control {
 		$this->json['label'] = $this->label;
 		$this->json['description'] = $this->description;
 		$this->json['instanceNumber'] = $this->instance_number;
+
+		if ( 'dropdown-pages' === $this->type ) {
+			$this->json['allow_addition'] = $this->allow_addition;
+		}
 	}
 
 	/**
@@ -554,10 +567,34 @@ class WP_Customize_Control {
 
 				// Hackily add in the data link parameter.
 				$dropdown = str_replace( '<select', '<select ' . $this->get_link(), $dropdown );
+
+				// Even more hacikly add auto-draft page stubs.
+				// @todo Eventually this should be removed in favor of the pages being injected into the underlying get_pages() call. See <https://github.com/xwp/wp-customize-posts/pull/250>.
+				$nav_menus_created_posts_setting = $this->manager->get_setting( 'nav_menus_created_posts' );
+				if ( $nav_menus_created_posts_setting && current_user_can( 'publish_pages' ) ) {
+					$auto_draft_page_options = '';
+					foreach ( $nav_menus_created_posts_setting->value() as $auto_draft_page_id ) {
+						$post = get_post( $auto_draft_page_id );
+						if ( $post && 'page' === $post->post_type ) {
+							$auto_draft_page_options .= sprintf( '<option value="%1$s">%2$s</option>', esc_attr( $post->ID ), esc_html( $post->post_title ) );
+						}
+					}
+					if ( $auto_draft_page_options ) {
+						$dropdown = str_replace( '</select>', $auto_draft_page_options . '</select>', $dropdown );
+					}
+				}
+
 				echo $dropdown;
 				?>
 				</label>
-				<?php
+				<?php if ( $this->allow_addition && current_user_can( 'publish_pages' ) && current_user_can( 'edit_theme_options' ) ) : // Currently tied to menus functionality. ?>
+					<button type="button" class="button add-new-toggle"><?php echo get_post_type_object( 'page' )->labels->add_new_item; ?></button>
+					<div class="new-content-item">
+						<label for="create-input-<?php echo $this->id; ?>"><span class="screen-reader-text"><?php _e( 'New page title' ); ?></span></label>
+						<input type="text" id="create-input-<?php echo $this->id; ?>" class="create-item-input" placeholder="<?php esc_attr_e( 'New page title&hellip;' ); ?>">
+						<button type="button" class="button add-content"><?php _e( 'Add' ); ?></button>
+					</div>
+				<?php endif;
 				break;
 			default:
 				?>
diff --git a/src/wp-includes/class-wp-customize-manager.php b/src/wp-includes/class-wp-customize-manager.php
index 5a7cd46421..229be36da6 100644
--- a/src/wp-includes/class-wp-customize-manager.php
+++ b/src/wp-includes/class-wp-customize-manager.php
@@ -3356,6 +3356,7 @@ final class WP_Customize_Manager {
 			'label' => __( 'Front page' ),
 			'section' => 'static_front_page',
 			'type' => 'dropdown-pages',
+			'allow_addition' => true,
 		) );
 
 		$this->add_setting( 'page_for_posts', array(
@@ -3367,6 +3368,7 @@ final class WP_Customize_Manager {
 			'label' => __( 'Posts page' ),
 			'section' => 'static_front_page',
 			'type' => 'dropdown-pages',
+			'allow_addition' => true,
 		) );
 
 		/* Custom CSS */
diff --git a/src/wp-includes/class-wp-customize-nav-menus.php b/src/wp-includes/class-wp-customize-nav-menus.php
index 2d9c13a40e..c8ef7a8a5f 100644
--- a/src/wp-includes/class-wp-customize-nav-menus.php
+++ b/src/wp-includes/class-wp-customize-nav-menus.php
@@ -370,6 +370,7 @@ final class WP_Customize_Nav_Menus {
 				'untitled'          => _x( '(no label)', 'missing menu item navigation label' ),
 				'unnamed'           => _x( '(unnamed)', 'Missing menu name.' ),
 				'custom_label'      => __( 'Custom Link' ),
+				'page_label'        => get_post_type_object( 'page' )->labels->singular_name,
 				/* translators: %s: menu location */
 				'menuLocation'      => _x( '(Currently set to: %s)', 'menu' ),
 				'menuNameLabel'     => __( 'Menu Name' ),
diff --git a/tests/phpunit/tests/customize/control.php b/tests/phpunit/tests/customize/control.php
index e6d1141219..ccd850ecc5 100644
--- a/tests/phpunit/tests/customize/control.php
+++ b/tests/phpunit/tests/customize/control.php
@@ -26,6 +26,7 @@ class Test_WP_Customize_Control extends WP_UnitTestCase {
 	 */
 	function setUp() {
 		parent::setUp();
+		wp_set_current_user( $this->factory()->user->create( array( 'role' => 'administrator' ) ) );
 		require_once( ABSPATH . WPINC . '/class-wp-customize-manager.php' );
 		// @codingStandardsIgnoreStart
 		$GLOBALS['wp_customize'] = new WP_Customize_Manager();
@@ -39,7 +40,6 @@ class Test_WP_Customize_Control extends WP_UnitTestCase {
 	 * @see WP_Customize_Control::check_capabilities()
 	 */
 	function test_check_capabilities() {
-		wp_set_current_user( self::factory()->user->create( array( 'role' => 'administrator' ) ) );
 		do_action( 'customize_register', $this->wp_customize );
 		$control = new WP_Customize_Control( $this->wp_customize, 'blogname', array(
 			'settings' => array( 'blogname' ),
@@ -77,6 +77,67 @@ class Test_WP_Customize_Control extends WP_UnitTestCase {
 		$this->assertTrue( $control->check_capabilities() );
 	}
 
+	/**
+	 * @ticket 38164
+	 */
+	function test_dropdown_pages() {
+		do_action( 'customize_register', $this->wp_customize );
+
+		$this->assertInstanceOf( 'WP_Customize_Nav_Menus', $this->wp_customize->nav_menus );
+		$nav_menus_created_posts_setting = $this->wp_customize->get_setting( 'nav_menus_created_posts' );
+		$this->assertInstanceOf( 'WP_Customize_Filter_Setting', $nav_menus_created_posts_setting );
+		$page_on_front_control = $this->wp_customize->get_control( 'page_on_front' );
+
+		// Ensure the add-new-toggle is absent if allow_addition param is not set.
+		$page_on_front_control->allow_addition = false;
+		ob_start();
+		$page_on_front_control->maybe_render();
+		$content = ob_get_clean();
+		$this->assertNotContains( 'add-new-toggle', $content );
+
+		// Ensure the add-new-toggle is absent if allow_addition param is set.
+		$page_on_front_control->allow_addition = true;
+		ob_start();
+		$page_on_front_control->maybe_render();
+		$content = ob_get_clean();
+		$this->assertContains( 'add-new-toggle', $content );
+
+		// Ensure that dropdown-pages delect is rendered even if there are no pages published (yet).
+		foreach ( get_pages() as $page ) {
+			wp_delete_post( $page->ID );
+		}
+		$page_on_front_control->allow_addition = true;
+		ob_start();
+		$page_on_front_control->maybe_render();
+		$content = ob_get_clean();
+		$this->assertContains( '<option value="0">', $content, 'Dropdown-pages renders select even without any pages published.' );
+
+		// Ensure that auto-draft pages are included if they are among the nav_menus_created_posts.
+		$auto_draft_page_id = $this->factory()->post->create( array(
+			'post_type' => 'page',
+			'post_status' => 'auto-draft',
+			'post_title' => 'Auto Draft Page',
+		) );
+		$this->factory()->post->create( array(
+			'post_type' => 'page',
+			'post_status' => 'auto-draft',
+			'post_title' => 'Orphan Auto Draft Page',
+		) );
+		$auto_draft_post_id = $this->factory()->post->create( array(
+			'post_type' => 'post',
+			'post_status' => 'auto-draft',
+			'post_title' => 'Auto Draft Post',
+		) );
+		$this->wp_customize->set_post_value( $nav_menus_created_posts_setting->id, array( $auto_draft_page_id, $auto_draft_post_id ) );
+		$nav_menus_created_posts_setting->preview();
+		ob_start();
+		$page_on_front_control->maybe_render();
+		$content = ob_get_clean();
+		$this->assertContains( sprintf( '<option value="%d">Auto Draft Page</option>', $auto_draft_page_id ), $content );
+		$this->assertNotContains( 'Auto Draft Post', $content );
+		$this->assertNotContains( 'Orphan Auto Draft Page', $content );
+	}
+
 	/**
 	 * Tear down.
 	 */