diff --git a/tests/phpunit/testdata/plugins/test-plugin-plugin-readme-multiple-parser-warnings/load.php b/tests/phpunit/testdata/plugins/test-plugin-plugin-readme-multiple-parser-warnings/load.php
new file mode 100644
index 000000000..22c15009d
--- /dev/null
+++ b/tests/phpunit/testdata/plugins/test-plugin-plugin-readme-multiple-parser-warnings/load.php
@@ -0,0 +1,16 @@
+<?php
+/**
+ * Plugin Name: Test Plugin Readme Errors (Multiple Parser Warnings)
+ * Plugin URI: https://github.com/WordPress/plugin-check
+ * Description: Test plugin for the Readme check.
+ * Requires at least: 6.0
+ * Requires PHP: 5.6
+ * Version: 1.0.0
+ * Author: WordPress Performance Team
+ * Author URI: https://make.wordpress.org/performance/
+ * License: GPLv2 or later
+ * License URI: https://www.gnu.org/licenses/old-licenses/gpl-2.0.html
+ * Text Domain: test-plugin-check-errors-multiple-parser-warnings
+ *
+ * @package test-plugin-check-errors-multiple-parser-warnings
+ */
diff --git a/tests/phpunit/testdata/plugins/test-plugin-plugin-readme-multiple-parser-warnings/readme.txt b/tests/phpunit/testdata/plugins/test-plugin-plugin-readme-multiple-parser-warnings/readme.txt
new file mode 100644
index 000000000..bab1907cd
--- /dev/null
+++ b/tests/phpunit/testdata/plugins/test-plugin-plugin-readme-multiple-parser-warnings/readme.txt
@@ -0,0 +1,12 @@
+=== Test Plugin Readme Errors Multiple Parser Warnings ===
+
+Contributors:      plugin-check, first name
+Requires at least: Previous
+Tested up to:      Latest
+Requires PHP:      PHP 5.6
+Stable tag:        1.0.0
+License:           GPLv2 or later
+License URI:       https://www.gnu.org/licenses/gpl-2.0.html
+Tags:              testing, security, plugin, readme, validation, enhancement, performance
+
+Lorem ipsum dolor sit amet, consectetur adipiscing elit. Integer vulputate nunc velit, vitae sollicitudin tortor viverra sed. Morbi sed nibh ex. Nulla vel augue velit. Maecenas vel lobortis orci. In eget metus dui. Vivamus eleifend volutpat diam. Duis viverra leo non eros auctor, nec placerat elit placerat. Nulla blandit odio risus. In eu dui non erat congue sagittis. Donec luctus tincidunt dolor, nec tempus erat pretium eu. Nunc a dictum odio. Vivamus vel faucibus lorem, eu finibus sem. Sed et vehicula ante, vel sodales augue. Donec tincidunt bibendum libero, ac tristique tellus rutrum nec. Curabitur viverra tincidunt eros non laoreet. Sed vitae consequat diam.
diff --git a/tests/phpunit/testdata/plugins/test-plugin-plugin-readme-parser-warnings/readme.txt b/tests/phpunit/testdata/plugins/test-plugin-plugin-readme-parser-warnings/readme.txt
index c71481201..5e3a03aca 100644
--- a/tests/phpunit/testdata/plugins/test-plugin-plugin-readme-parser-warnings/readme.txt
+++ b/tests/phpunit/testdata/plugins/test-plugin-plugin-readme-parser-warnings/readme.txt
@@ -3,7 +3,7 @@
 
 Contributors:      plugin-check
 Requires at least: 6.0
-Tested up to:      Latest
+Tested up to:      6.1
 Requires PHP:      PHP 5.6
 Stable tag:        1.0.0
 License:           GPLv2 or later
diff --git a/tests/phpunit/tests/Checker/Checks/Plugin_Readme_Check_Tests.php b/tests/phpunit/tests/Checker/Checks/Plugin_Readme_Check_Tests.php
index ddbe512d1..adb6a282a 100644
--- a/tests/phpunit/tests/Checker/Checks/Plugin_Readme_Check_Tests.php
+++ b/tests/phpunit/tests/Checker/Checks/Plugin_Readme_Check_Tests.php
@@ -233,15 +233,60 @@ public function test_run_with_errors_parser_warnings() {
 
 		$this->assertNotEmpty( $warnings );
 		$this->assertArrayHasKey( 'readme.txt', $warnings );
-		$this->assertEquals( 2, $check_result->get_warning_count() );
+		$this->assertEquals( 1, $check_result->get_warning_count() );
 
-		// Check for parser warnings.
+		// Check for parser warning.
 		$this->assertArrayHasKey( 0, $warnings['readme.txt'] );
 		$this->assertArrayHasKey( 0, $warnings['readme.txt'][0] );
 		$this->assertArrayHasKey( 'code', $warnings['readme.txt'][0][0][0] );
 		$this->assertEquals( 'readme_parser_warnings', $warnings['readme.txt'][0][0][0]['code'] );
-		$this->assertArrayHasKey( 'code', $warnings['readme.txt'][0][0][1] );
-		$this->assertEquals( 'readme_parser_warnings', $warnings['readme.txt'][0][0][1]['code'] );
+	}
+
+	public function test_run_with_errors_multiple_parser_warnings() {
+		$readme_check  = new Plugin_Readme_Check();
+		$check_context = new Check_Context( UNIT_TESTS_PLUGIN_DIR . 'test-plugin-plugin-readme-multiple-parser-warnings/load.php' );
+		$check_result  = new Check_Result( $check_context );
+
+		$readme_check->run( $check_result );
+
+		$errors   = $check_result->get_errors();
+		$warnings = $check_result->get_warnings();
+
+		$this->assertNotEmpty( $warnings );
+		$this->assertArrayHasKey( 'readme.txt', $warnings );
+		$this->assertEquals( 6, $check_result->get_warning_count() );
+		$this->assertEmpty( $errors );
+		$this->assertEquals( 0, $check_result->get_error_count() );
+
+		// Check for parser warnings.
+		$this->assertArrayHasKey( 0, $warnings['readme.txt'] );
+		$this->assertArrayHasKey( 0, $warnings['readme.txt'][0] );
+
+		for ( $i = 0; $i < 6; ++$i ) {
+			$this->assertArrayHasKey( 'code', $warnings['readme.txt'][0][0][ $i ] );
+			$this->assertEquals( 'readme_parser_warnings', $warnings['readme.txt'][0][0][ $i ]['code'] );
+		}
+	}
+
+	public function test_run_with_errors_multiple_parser_warnings_and_empty_ignored_array() {
+		add_filter( 'wp_plugin_check_ignored_readme_warnings', '__return_empty_array' );
+
+		$readme_check  = new Plugin_Readme_Check();
+		$check_context = new Check_Context( UNIT_TESTS_PLUGIN_DIR . 'test-plugin-plugin-readme-multiple-parser-warnings/load.php' );
+		$check_result  = new Check_Result( $check_context );
+
+		$readme_check->run( $check_result );
+
+		$errors   = $check_result->get_errors();
+		$warnings = $check_result->get_warnings();
+
+		$this->assertNotEmpty( $warnings );
+		$this->assertArrayHasKey( 'readme.txt', $warnings );
+		$this->assertEquals( 7, $check_result->get_warning_count() );
+		$this->assertEmpty( $errors );
+		$this->assertEquals( 0, $check_result->get_error_count() );
+
+		remove_filter( 'wp_plugin_check_ignored_readme_warnings', '__return_empty_array' );
 	}
 
 	public function test_filter_readme_warnings_ignored() {
@@ -277,7 +322,6 @@ public function test_filter_wp_plugin_check_ignored_readme_warnings_will_return_
 		$custom_ignores = array(
 			'requires_php_header_ignored',
 			'contributor_ignored',
-			'tested_header_ignored',
 		);
 
 		// Create a mock filter that will return our custom ignores.