diff --git a/src/wp-includes/option.php b/src/wp-includes/option.php
index 58c4113ffc..d2ffa675b1 100644
--- a/src/wp-includes/option.php
+++ b/src/wp-includes/option.php
@@ -859,11 +859,30 @@ function update_option( $option, $value, $autoload = null ) {
 	}
 
 	if ( ! wp_installing() ) {
-		$alloptions = wp_load_alloptions( true );
-		if ( isset( $alloptions[ $option ] ) ) {
+		if ( ! isset( $update_args['autoload'] ) ) {
+			// Update the cached value based on where it is currently cached.
+			$alloptions = wp_load_alloptions( true );
+			if ( isset( $alloptions[ $option ] ) ) {
+				$alloptions[ $option ] = $serialized_value;
+				wp_cache_set( 'alloptions', $alloptions, 'options' );
+			} else {
+				wp_cache_set( $option, $serialized_value, 'options' );
+			}
+		} elseif ( 'yes' === $update_args['autoload'] ) {
+			// Delete the individual cache, then set in alloptions cache.
+			wp_cache_delete( $option, 'options' );
+
+			$alloptions = wp_load_alloptions( true );
 			$alloptions[ $option ] = $serialized_value;
 			wp_cache_set( 'alloptions', $alloptions, 'options' );
 		} else {
+			// Delete the alloptions cache, then set the individual cache.
+			$alloptions = wp_load_alloptions( true );
+			if ( isset( $alloptions[ $option ] ) ) {
+				unset( $alloptions[ $option ] );
+				wp_cache_set( 'alloptions', $alloptions, 'options' );
+			}
+
 			wp_cache_set( $option, $serialized_value, 'options' );
 		}
 	}
diff --git a/tests/phpunit/tests/option/option.php b/tests/phpunit/tests/option/option.php
index ae4b0e71f6..04b89c4429 100644
--- a/tests/phpunit/tests/option/option.php
+++ b/tests/phpunit/tests/option/option.php
@@ -777,4 +777,36 @@ class Tests_Option_Option extends WP_UnitTestCase {
 		// Assert that the filter is still present.
 		$this->assertSame( 10, has_filter( 'pre_option_foo', '__return_zero' ) );
 	}
+
+	/**
+	 * Tests that calling update_option() with changed autoload from 'no' to 'yes' updates the cache correctly.
+	 *
+	 * This ensures that no stale data is served in case the option is deleted after.
+	 *
+	 * @ticket 51352
+	 *
+	 * @covers ::update_option
+	 */
+	public function test_update_option_with_autoload_change_no_to_yes() {
+		add_option( 'foo', 'value1', '', 'no' );
+		update_option( 'foo', 'value2', 'yes' );
+		delete_option( 'foo' );
+		$this->assertFalse( get_option( 'foo' ) );
+	}
+
+	/**
+	 * Tests that calling update_option() with changed autoload from 'yes' to 'no' updates the cache correctly.
+	 *
+	 * This ensures that no stale data is served in case the option is deleted after.
+	 *
+	 * @ticket 51352
+	 *
+	 * @covers ::update_option
+	 */
+	public function test_update_option_with_autoload_change_yes_to_no() {
+		add_option( 'foo', 'value1', '', 'yes' );
+		update_option( 'foo', 'value2', 'no' );
+		delete_option( 'foo' );
+		$this->assertFalse( get_option( 'foo' ) );
+	}
 }