diff --git a/src/wp-admin/includes/class-wp-list-table.php b/src/wp-admin/includes/class-wp-list-table.php
index 0c5e21bde3..8df48e6a0c 100644
--- a/src/wp-admin/includes/class-wp-list-table.php
+++ b/src/wp-admin/includes/class-wp-list-table.php
@@ -1108,7 +1108,10 @@ class WP_List_Table {
 	 */
 	protected function get_column_info() {
 		// $_column_headers is already set / cached.
-		if ( isset( $this->_column_headers ) && is_array( $this->_column_headers ) ) {
+		if (
+			isset( $this->_column_headers ) &&
+			is_array( $this->_column_headers )
+		) {
 			/*
 			 * Backward compatibility for `$_column_headers` format prior to WordPress 4.3.
 			 *
@@ -1116,12 +1119,18 @@ class WP_List_Table {
 			 * column headers property. This ensures the primary column name is included
 			 * in plugins setting the property directly in the three item format.
 			 */
+			if ( 4 === count( $this->_column_headers ) ) {
+				return $this->_column_headers;
+			}
+
 			$column_headers = array( array(), array(), array(), $this->get_primary_column_name() );
 			foreach ( $this->_column_headers as $key => $value ) {
 				$column_headers[ $key ] = $value;
 			}
 
-			return $column_headers;
+			$this->_column_headers = $column_headers;
+
+			return $this->_column_headers;
 		}
 
 		$columns = get_column_headers( $this->screen );
diff --git a/tests/phpunit/tests/admin/wpListTable.php b/tests/phpunit/tests/admin/wpListTable.php
new file mode 100644
index 0000000000..c07d7579c8
--- /dev/null
+++ b/tests/phpunit/tests/admin/wpListTable.php
@@ -0,0 +1,107 @@
+<?php
+
+/**
+ * @group admin
+ *
+ * @covers WP_List_Table
+ */
+class Tests_Admin_WpListTable extends WP_UnitTestCase {
+
+	/**
+	 * Tests that `WP_List_Table::get_column_info()` only adds the primary
+	 * column header when necessary.
+	 *
+	 * @ticket 34564
+	 *
+	 * @dataProvider data_should_only_add_primary_column_when_needed
+	 *
+	 * @covers WP_List_Table::get_column_info
+	 *
+	 * @param string $list_class          The name of the WP_List_Table child class.
+	 * @param array  $headers             A list of column headers.
+	 * @param array  $expected            The expected column headers.
+	 * @param int    $expected_hook_count The expected number of times the hook is called.
+	 */
+	public function test_should_only_add_primary_column_when_needed( $list_class, $headers, $expected, $expected_hook_count ) {
+		$hook = new MockAction();
+		add_filter( 'list_table_primary_column', array( $hook, 'filter' ) );
+
+		/*
+		 * Set a dummy value for the current screen in the admin to prevent
+		 * `_get_list_table()` throwing.
+		 */
+		$GLOBALS['hook_suffix'] = 'my-hook';
+
+		$list_table = _get_list_table( $list_class );
+
+		$column_headers = new ReflectionProperty( $list_table, '_column_headers' );
+		$column_headers->setAccessible( true );
+		$column_headers->setValue( $list_table, $headers );
+
+		$column_info = new ReflectionMethod( $list_table, 'get_column_info' );
+		$column_info->setAccessible( true );
+
+		$this->assertSame( $expected, $column_info->invoke( $list_table ), 'The actual columns did not match the expected columns' );
+		$this->assertSame( $expected_hook_count, $hook->get_call_count(), 'The hook was not called the expected number of times' );
+	}
+
+	/**
+	 * Data provider.
+	 *
+	 * @return array
+	 */
+	public function data_should_only_add_primary_column_when_needed() {
+		/*
+		 * `WP_Post_Comments_List_Table` overrides `get_column_info()` rather than
+		 * use the default `WP_List_Table::get_column_info()`. Therefore it is
+		 * untested.
+		 */
+		$list_primary_columns = array(
+			'WP_Application_Passwords_List_Table'         => 'name',
+			'WP_Comments_List_Table'                      => 'author',
+			'WP_Links_List_Table'                         => 'name',
+			'WP_Media_List_Table'                         => 'title',
+			'WP_MS_Sites_List_Table'                      => 'blogname',
+			'WP_MS_Themes_List_Table'                     => 'name',
+			'WP_MS_Users_List_Table'                      => 'username',
+			'WP_Plugin_Install_List_Table'                => '',
+			'WP_Plugins_List_Table'                       => 'name',
+			'WP_Posts_List_Table'                         => 'title',
+			'WP_Privacy_Data_Export_Requests_List_Table'  => 'email',
+			'WP_Privacy_Data_Removal_Requests_List_Table' => 'email',
+			'WP_Terms_List_Table'                         => 'name',
+			'WP_Theme_Install_List_Table'                 => '',
+			'WP_Themes_List_Table'                        => '',
+			'WP_Users_List_Table'                         => 'username',
+		);
+
+		$datasets = array();
+
+		foreach ( $list_primary_columns as $list_class => $primary_column ) {
+			$datasets[ $list_class . ' - three columns' ] = array(
+				'list_class'          => $list_class,
+				'headers'             => array( 'First', 'Second', 'Third' ),
+				'expected'            => array( 'First', 'Second', 'Third', $primary_column ),
+				'expected_hook_count' => 1,
+			);
+
+			$datasets[ $list_class . ' - four columns' ] = array(
+				'list_class'          => $list_class,
+				'headers'             => array( 'First', 'Second', 'Third', 'Fourth' ),
+				'expected'            => array( 'First', 'Second', 'Third', 'Fourth' ),
+				'expected_hook_count' => 0,
+			);
+		}
+
+		/*
+		 * `WP_MS_Themes_List_Table` and `WP_Plugins_List_Table` override the
+		 * `get_primary_column_name()` method rather than use the default
+		 * `WP_List_Table::get_primary_column_name()`. Neither include the
+		 * `list_table_primary_column` hook.
+		 */
+		$datasets['WP_MS_Themes_List_Table - three columns']['expected_hook_count'] = 0;
+		$datasets['WP_Plugins_List_Table - three columns']['expected_hook_count']   = 0;
+
+		return $datasets;
+	}
+}