diff --git a/src/js/media/models/attachment.js b/src/js/media/models/attachment.js
index 267624b7d6c48..6c525cb32e76b 100644
--- a/src/js/media/models/attachment.js
+++ b/src/js/media/models/attachment.js
@@ -71,9 +71,14 @@ Attachment = Backbone.Model.extend(/** @lends wp.media.model.Attachment.prototyp
 		} else if ( 'delete' === method ) {
 			options = options || {};
 
-			if ( ! options.wait ) {
-				this.destroyed = true;
-			}
+			/*
+			 * Mark as destroyed before the request so mirrored collections
+			 * filter it out when the `destroy` event fires. With `wait: true`,
+			 * Backbone triggers `destroy` before the request's `done` handler,
+			 * so setting the flag there was too late and the deleted item
+			 * lingered in the grid. Restored on failure. See #65513.
+			 */
+			this.destroyed = true;
 
 			options.context = this;
 			options.data = _.extend( options.data || {}, {
@@ -82,9 +87,7 @@ Attachment = Backbone.Model.extend(/** @lends wp.media.model.Attachment.prototyp
 				_wpnonce: this.get('nonces')['delete']
 			});
 
-			return wp.media.ajax( options ).done( function() {
-				this.destroyed = true;
-			}).fail( function() {
+			return wp.media.ajax( options ).fail( function() {
 				this.destroyed = false;
 			});
 
diff --git a/src/js/media/models/attachments.js b/src/js/media/models/attachments.js
index 23510bd949f4c..2189cab66c611 100644
--- a/src/js/media/models/attachments.js
+++ b/src/js/media/models/attachments.js
@@ -204,7 +204,7 @@ var Attachments = Backbone.Collection.extend(/** @lends wp.media.model.Attachmen
 	 * Start observing another attachments collection change events
 	 * and replicate them on this collection.
 	 *
-	 * @param {wp.media.model.Attachments} The attachments collection to observe.
+	 * @param {wp.media.model.Attachments} attachments The attachments collection to observe.
 	 * @return {wp.media.model.Attachments} Returns itself to allow chaining.
 	 */
 	observe: function( attachments ) {
@@ -212,9 +212,18 @@ var Attachments = Backbone.Collection.extend(/** @lends wp.media.model.Attachmen
 		this.observers.push( attachments );
 
 		attachments.on( 'add change remove', this._validateHandler, this );
-		attachments.on( 'add', this._addToTotalAttachments, this );
-		attachments.on( 'remove', this._removeFromTotalAttachments, this );
 		attachments.on( 'reset', this._validateAllHandler, this );
+
+		/*
+		 * Only count the mirrored query collection. Counting other observed
+		 * collections such as the selection double-counts an uploaded image
+		 * that is also auto-selected, breaking the count. See #65513.
+		 */
+		if ( attachments === this.mirroring ) {
+			attachments.on( 'add', this._addToTotalAttachments, this );
+			attachments.on( 'remove', this._removeFromTotalAttachments, this );
+		}
+
 		this.validateAll( attachments );
 		return this;
 	},
@@ -239,7 +248,7 @@ var Attachments = Backbone.Collection.extend(/** @lends wp.media.model.Attachmen
 		return this;
 	},
 	/**
-	 * Update total attachment count when items are added to a collection.
+	 * Update total attachment count when items are removed from a collection.
 	 *
 	 * @access private
 	 *
diff --git a/tests/e2e/specs/featured-image-modal.test.js b/tests/e2e/specs/featured-image-modal.test.js
new file mode 100644
index 0000000000000..0068d5acd6437
--- /dev/null
+++ b/tests/e2e/specs/featured-image-modal.test.js
@@ -0,0 +1,79 @@
+/**
+ * WordPress dependencies
+ */
+import { test, expect } from '@wordpress/e2e-test-utils-playwright';
+
+/**
+ * External dependencies
+ */
+import path from 'path';
+
+const TEST_IMAGE = path.join(
+	__dirname,
+	'..',
+	'..',
+	'phpunit',
+	'data',
+	'images',
+	'test-image-1-100x100.jpg'
+);
+
+/**
+ * @see https://core.trac.wordpress.org/ticket/65513
+ */
+test.describe( 'Featured image modal media count and deletion', () => {
+	test.beforeEach( async ( { requestUtils } ) => {
+		// Start from an empty Media Library so the count is deterministic.
+		await requestUtils.deleteAllMedia();
+	} );
+
+	test.afterEach( async ( { requestUtils } ) => {
+		await requestUtils.deleteAllMedia();
+	} );
+
+	test( 'reports the correct count on first upload and removes a deleted item from the grid', async ( {
+		page,
+		admin,
+	} ) => {
+		await admin.createNewPost( { showWelcomeGuide: false } );
+
+		// `wp.media` is enqueued on the post editing screen.
+		await page.waitForFunction(
+			() => window.wp && window.wp.media && window.wp.media.featuredImage
+		);
+
+		// The Featured Image modal opens on the Upload tab.
+		await page.evaluate( () => window.wp.media.featuredImage.frame().open() );
+
+		const modal = page.locator( '.media-modal' );
+		await expect( modal ).toBeVisible();
+
+		await modal
+			.locator( 'input[type="file"]' )
+			.setInputFiles( TEST_IMAGE );
+
+		await page.evaluate( () => window.wp.media.frame.content.mode( 'browse' ) );
+
+		await expect(
+			modal.locator( '.attachments .attachment' )
+		).toHaveCount( 1 );
+
+		// The uploaded image must be counted once, not once per collection it
+		// belongs to (mirrored query + auto-selected selection).
+		await expect( modal.locator( '.load-more-count' ) ).toHaveText(
+			'Showing 1 of 1 media items'
+		);
+
+		page.on( 'dialog', ( dialog ) => dialog.accept() );
+
+		// The uploaded image is auto-selected, so its details are already shown.
+		await modal
+			.locator( '.attachment-details .delete-attachment' )
+			.click();
+
+		// The deleted attachment must not linger in the grid.
+		await expect(
+			modal.locator( '.attachments .attachment' )
+		).toHaveCount( 0 );
+	} );
+} );