diff --git a/src/js/_enqueues/admin/postbox.js b/src/js/_enqueues/admin/postbox.js
index 452e95b26c..1fdf0ebeb8 100644
--- a/src/js/_enqueues/admin/postbox.js
+++ b/src/js/_enqueues/admin/postbox.js
@@ -7,10 +7,11 @@
  * @output wp-admin/js/postbox.js
  */
 
-/* global ajaxurl, postBoxL10n, postboxes */
+/* global ajaxurl, postboxes */
 
 (function($) {
-	var $document = $( document );
+	var $document = $( document ),
+		__ = wp.i18n.__;
 
 	/**
 	 * This object contains all function to handle the behaviour of the post boxes. The post boxes are the boxes you see
@@ -235,14 +236,18 @@
 						.end();
 				},
 				opacity: 0.65,
+				start: function() {
+					$( 'body' ).addClass( 'is-dragging-metaboxes' );
+				},
 				stop: function() {
 					var $el = $( this );
 
+					$( 'body' ).removeClass( 'is-dragging-metaboxes' );
+
 					if ( $el.find( '#dashboard_browser_nag' ).is( ':visible' ) && 'dashboard_browser_nag' != this.firstChild.id ) {
 						$el.sortable('cancel');
 						return;
 					}
-
 					postboxes.save_order(page);
 				},
 				receive: function(e,ui) {
@@ -345,26 +350,44 @@
 		 * @return {void}
 		 */
 		_mark_area : function() {
-			var visible = $('div.postbox:visible').length, side = $('#post-body #side-sortables');
+			var visibleSortables = $( '#dashboard-widgets .meta-box-sortables:visible, #post-body .meta-box-sortables:visible' ),
+				areAllVisibleSortablesEmpty = true;
 
-			$( '#dashboard-widgets .meta-box-sortables:visible' ).each( function() {
+			visibleSortables.each( function() {
 				var t = $(this);
 
-				if ( visible == 1 || t.children('.postbox:visible').length ) {
+				if ( t.children('.postbox:visible').length ) {
 					t.removeClass('empty-container');
+					areAllVisibleSortablesEmpty = false;
 				}
 				else {
 					t.addClass('empty-container');
-					t.attr('data-emptyString', postBoxL10n.postBoxEmptyString);
 				}
 			});
 
-			if ( side.length ) {
-				if ( side.children('.postbox:visible').length )
-					side.removeClass('empty-container');
-				else if ( $('#postbox-container-1').css('width') == '280px' )
-					side.addClass('empty-container');
+			postboxes.updateEmptySortablesText( visibleSortables, areAllVisibleSortablesEmpty );
+		},
+
+		/**
+		 * Updates the text for the empty sortable areas on the Dashboard.
+		 *
+		 * @since 5.5.0
+		 *
+		 * @return {void}
+		 */
+		updateEmptySortablesText: function( visibleSortables, areAllVisibleSortablesEmpty ) {
+			var isDashboard = $( '#dashboard-widgets' ).length,
+				emptySortableText = areAllVisibleSortablesEmpty ?  __( 'Add boxes from the Screen Options menu' ) : __( 'Drag boxes here' );
+
+			if ( ! isDashboard ) {
+				return;
 			}
+
+			visibleSortables.each( function() {
+				if ( $( this ).hasClass( 'empty-container' ) ) {
+					$( this ).attr( 'data-emptyString', emptySortableText );
+				}
+			} );
 		},
 
 		/**
diff --git a/src/wp-admin/css/common.css b/src/wp-admin/css/common.css
index 095593590f..ba9bcb9ad9 100644
--- a/src/wp-admin/css/common.css
+++ b/src/wp-admin/css/common.css
@@ -29,46 +29,6 @@
 	overflow: visible;
 }
 
-/* inner 2 column liquid layout */
-
-.inner-sidebar {
-	float: right;
-	clear: right;
-	display: none;
-	width: 281px;
-	position: relative;
-}
-
-.columns-2 .inner-sidebar {
-	margin-right: auto;
-	width: 286px;
-	display: block;
-}
-
-.inner-sidebar #side-sortables,
-.columns-2 .inner-sidebar #side-sortables {
-	min-height: 300px;
-	width: 280px;
-	padding: 0;
-}
-
-.has-right-sidebar .inner-sidebar {
-	display: block;
-}
-
-.has-right-sidebar #post-body {
-	float: left;
-	clear: left;
-	width: 100%;
-	margin-right: -2000px;
-}
-
-.has-right-sidebar #post-body-content {
-	margin-right: 300px;
-	float: none;
-	width: auto;
-}
-
 /* 2 columns main area */
 
 #col-left {
@@ -1983,36 +1943,11 @@ html.wp-toolbar {
 }
 
 .metabox-holder .postbox-container .empty-container {
-	border: 3px dashed #b4b9be;
+	outline: 3px dashed #b4b9be;
 	height: 250px;
 	position: relative;
 }
 
-.metabox-holder .postbox-container .empty-container:after {
-	content: attr(data-emptystring);
-	margin: auto;
-	position: absolute;
-	top: 0;
-	left: 0;
-	bottom: 0;
-	right: 0;
-	height: 1em;
-	width: 200px;
-	text-align: center;
-	color: #ccc;
-	font-size: 18px;
-	display: none;
-}
-
-.metabox-holder.columns-1 .postbox-container .empty-container,
-.columns-2 #postbox-container-3 .empty-container,
-.columns-2 #postbox-container-4 .empty-container,
-.columns-3 #postbox-container-4 .empty-container {
-	border: 0 none;
-	height: 0;
-	min-height: 0;
-}
-
 #post-body-content {
 	width: 100%;
 	min-width: 463px;
@@ -2032,7 +1967,7 @@ html.wp-toolbar {
 /* one column on the dash */
 @media only screen and (max-width: 799px) {
 	#wpbody-content .metabox-holder .postbox-container .empty-container {
-		border: 0 none;
+		outline: none;
 		height: 0;
 		min-height: 0;
 	}
diff --git a/src/wp-admin/css/dashboard.css b/src/wp-admin/css/dashboard.css
index 6160ee3d09..91604459bb 100644
--- a/src/wp-admin/css/dashboard.css
+++ b/src/wp-admin/css/dashboard.css
@@ -48,10 +48,35 @@
 }
 
 #dashboard-widgets .meta-box-sortables {
-	margin: 0 8px;
+	/* Required min-height to make the jQuery UI Sortable drop zone work. */
 	min-height: 100px;
+	margin: 0 8px 20px;
 }
 
+/* Only highlight drop zones when dragging and only in the 2 columns layout. */
+.is-dragging-metaboxes #dashboard-widgets .meta-box-sortables {
+	outline: 3px dashed #606a73;
+	/* Prevent margin on the child from collapsing with margin on the parent. */
+	display: flow-root;
+}
+
+#dashboard-widgets .postbox-container .empty-container:after {
+	content: attr(data-emptystring);
+	margin: auto;
+	position: absolute;
+	top: 50%;
+	left: 0;
+	right: 0;
+	transform: translateY( -50% );
+	padding: 0 2em;
+	text-align: center;
+	color: #606a73;
+	font-size: 16px;
+	line-height: 1.5;
+	display: none;
+}
+
+
 /* @todo: this was originally in this section, but likely belongs elsewhere */
 #the-comment-list td.comment p.comment-author {
 	margin-top: 0;
@@ -1078,6 +1103,18 @@ a.rsswidget {
 	#wpbody-content #dashboard-widgets .postbox-container {
 		width: 100%;
 	}
+
+	#dashboard-widgets .meta-box-sortables {
+		min-height: 0;
+	}
+
+	.is-dragging-metaboxes #dashboard-widgets .meta-box-sortables {
+		min-height: 100px;
+	}
+
+	#dashboard-widgets .meta-box-sortables.empty-container {
+		margin-bottom: 0;
+	}
 }
 
 /* two columns on the dash, but keep the setting if one is selected */
@@ -1095,9 +1132,10 @@ a.rsswidget {
 
 	#dashboard-widgets #postbox-container-3 .empty-container,
 	#dashboard-widgets #postbox-container-4 .empty-container {
-		border: 0 none;
+		outline: none;
 		height: 0;
 		min-height: 0;
+		margin-bottom: 0;
 	}
 
 	#dashboard-widgets #postbox-container-3 .empty-container:after,
@@ -1109,10 +1147,11 @@ a.rsswidget {
 		width: 100%;
 	}
 
-	#wpbody #wpbody-content .metabox-holder.columns-1 .postbox-container .empty-container {
-		border: 0 none;
+	#wpbody #dashboard-widgets .metabox-holder.columns-1 .postbox-container .empty-container {
+		outline: none;
 		height: 0;
 		min-height: 0;
+		margin-bottom: 0;
 	}
 
 	/* show the radio buttons for column prefs only for one or two columns */
@@ -1126,7 +1165,7 @@ a.rsswidget {
 		display: none;
 	}
 
-	.metabox-holder .postbox-container .empty-container:after {
+	#dashboard-widgets .postbox-container .empty-container:after {
 		display: block;
 	}
 }
@@ -1147,16 +1186,24 @@ a.rsswidget {
 	}
 
 	#dashboard-widgets #postbox-container-4 .empty-container {
-		border: 0 none;
+		outline: none;
 		height: 0;
 		min-height: 0;
+		margin-bottom: 0;
 	}
 
 	#dashboard-widgets #postbox-container-4 .empty-container:after {
 		display: none;
 	}
 
-	.metabox-holder .postbox-container .empty-container:after {
+	#dashboard-widgets .postbox-container .empty-container:after {
+		display: block;
+	}
+}
+
+/* Always show the "Drag boxes here" CSS generated content on large screens. */
+@media only screen and (min-width: 1801px) {
+	#dashboard-widgets .postbox-container .empty-container:after {
 		display: block;
 	}
 }
diff --git a/src/wp-admin/css/edit.css b/src/wp-admin/css/edit.css
index 54884f1c94..a65f7ab063 100644
--- a/src/wp-admin/css/edit.css
+++ b/src/wp-admin/css/edit.css
@@ -147,8 +147,37 @@ body.post-new-php .submitbox .submitdelete {
 }
 
 /* Post Screen */
-#post-body #normal-sortables {
-	min-height: 50px;
+
+/* Only target the sortables in the post screen excluding the ones in the Dashboard. */
+#post-body .meta-box-sortables {
+	/* Required min-height to make the jQuery UI Sortable drop zone work. */
+	min-height: 1px;
+}
+
+/* Resets height and outline inherited from common.css. */
+#post-body.columns-1 #side-sortables.empty-container,
+#post-body #normal-sortables.empty-container,
+#post-body #advanced-sortables.empty-container {
+	/* Sortables need some initial height to work correctly. */
+	height: 1px;
+	outline: none;
+}
+
+/* Only highlight drop zones when dragging and only in the 2 columns layout. */
+.is-dragging-metaboxes #post-body.columns-2 #side-sortables,
+.is-dragging-metaboxes #post-body #normal-sortables,
+.is-dragging-metaboxes #post-body #advanced-sortables {
+	outline: 3px dashed #606a73;
+	/* Prevent margin on the child from collapsing with margin on the parent. */
+	display: flow-root;
+	/*
+	 * This min-height is meant to limit jumpiness while dragging. It's equivalent
+	 * to the minimum height of the sortable-placeholder which is given by the height
+	 * of a collapsed post box (36px + 1px top and bottom borders) + the placeholder
+	 * bottom margin (20px) + 2 additional pixels to compensate browsers rounding.
+	 */
+	min-height: 60px;
+	margin-bottom: 20px;
 }
 
 .postbox {
@@ -1453,7 +1482,10 @@ table.links-table {
 	}
 }
 
-/* one column on the attachment editor screen */
+/*
+ * The edit attachment screen auto-switches to one column layout when the
+ * viewport is smaller than 1200 pixels.
+ */
 @media only screen and (max-width: 1200px) {
 	.post-type-attachment #poststuff {
 		min-width: 0;
@@ -1470,7 +1502,7 @@ table.links-table {
 
 	.post-type-attachment #poststuff #postbox-container-1 .empty-container,
 	.post-type-attachment #poststuff #postbox-container-1 #side-sortables:empty {
-		border: 0 none;
+		outline: none;
 		height: 0;
 		min-height: 0;
 	}
@@ -1480,6 +1512,12 @@ table.links-table {
 		width: auto;
 	}
 
+	.is-dragging-metaboxes.post-type-attachment #post-body .meta-box-sortables {
+		outline: none;
+		min-height: 0;
+		margin-bottom: 0;
+	}
+
 	/* hide the radio buttons for column prefs */
 	.post-type-attachment .screen-layout,
 	.post-type-attachment .columns-prefs {
@@ -1504,7 +1542,7 @@ table.links-table {
 
 	#poststuff #postbox-container-1 .empty-container,
 	#poststuff #postbox-container-1 #side-sortables:empty {
-		border: 0 none;
+		outline: none;
 		height: 0;
 		min-height: 0;
 	}
diff --git a/src/wp-includes/script-loader.php b/src/wp-includes/script-loader.php
index 0f8cfb0fd8..1b44067c8a 100644
--- a/src/wp-includes/script-loader.php
+++ b/src/wp-includes/script-loader.php
@@ -1240,13 +1240,7 @@ function wp_default_scripts( $scripts ) {
 		$scripts->add( 'xfn', "/wp-admin/js/xfn$suffix.js", array( 'jquery' ), false, 1 );
 
 		$scripts->add( 'postbox', "/wp-admin/js/postbox$suffix.js", array( 'jquery-ui-sortable' ), false, 1 );
-		did_action( 'init' ) && $scripts->localize(
-			'postbox',
-			'postBoxL10n',
-			array(
-				'postBoxEmptyString' => __( 'Drag boxes here' ),
-			)
-		);
+		$scripts->set_translations( 'postbox' );
 
 		$scripts->add( 'tags-box', "/wp-admin/js/tags-box$suffix.js", array( 'jquery', 'tags-suggest' ), false, 1 );