diff --git a/packages/mysql-on-sqlite/src/sqlite/class-wp-mysql-on-sqlite.php b/packages/mysql-on-sqlite/src/sqlite/class-wp-mysql-on-sqlite.php
index eee3f050b..ab466f00d 100644
--- a/packages/mysql-on-sqlite/src/sqlite/class-wp-mysql-on-sqlite.php
+++ b/packages/mysql-on-sqlite/src/sqlite/class-wp-mysql-on-sqlite.php
@@ -5779,6 +5779,27 @@ private function recreate_table_from_information_schema(
 			)
 		);
 
+		// Preserve the AUTO_INCREMENT counter from the original table.
+		$schema             = $table_is_temporary ? 'temp' : 'main';
+		$has_sequence_table = (bool) $this->execute_sqlite_query(
+			sprintf( "SELECT 1 FROM %s.sqlite_master WHERE type = 'table' AND name = 'sqlite_sequence'", $schema )
+		)->fetchColumn();
+		if ( $has_sequence_table ) {
+			$this->execute_sqlite_query(
+				sprintf(
+					'UPDATE %s.sqlite_sequence
+					SET seq = MAX(seq, COALESCE((
+						SELECT seq FROM %s.sqlite_sequence
+						WHERE name = ? COLLATE NOCASE -- $table_name: original table
+					), 0))
+					WHERE name = ? -- $tmp_table_name: update only the replacement\'s row.',
+					$schema,
+					$schema
+				),
+				array( $table_name, $tmp_table_name )
+			);
+		}
+
 		// 4. Drop the original table.
 		$this->execute_sqlite_query( sprintf( 'DROP TABLE %s', $quoted_table_name ) );
 
diff --git a/packages/mysql-on-sqlite/tests/WP_MySQL_On_SQLite_Metadata_Tests.php b/packages/mysql-on-sqlite/tests/WP_MySQL_On_SQLite_Metadata_Tests.php
index 1366cb840..c3305dec5 100644
--- a/packages/mysql-on-sqlite/tests/WP_MySQL_On_SQLite_Metadata_Tests.php
+++ b/packages/mysql-on-sqlite/tests/WP_MySQL_On_SQLite_Metadata_Tests.php
@@ -929,6 +929,149 @@ public function testAlterTableSetAutoIncrement(): void {
 		$this->assertSame( null, $result[0]->Auto_increment );
 	}
 
+	/**
+	 * @dataProvider tableRebuildsWithAutoIncrement
+	 */
+	public function testTableRebuildPreservesAutoIncrement( string $temporary, string $rebuild, array $setup, string $expected_id ): void {
+		$this->assertQuery( "CREATE $temporary TABLE t (id BIGINT AUTO_INCREMENT PRIMARY KEY, name TEXT)" );
+		foreach ( $setup as $query ) {
+			$this->assertQuery( $query );
+		}
+		$rows = $this->assertQuery( 'SELECT * FROM t ORDER BY id' );
+
+		$result = $this->assertQuery( $rebuild );
+		if ( is_array( $result ) ) {
+			$this->assertSame( 'OK', $result[0]->Msg_text );
+		}
+		$this->assertEquals( $rows, $this->assertQuery( 'SELECT id, name FROM t ORDER BY id' ) );
+		if ( '' === $temporary ) {
+			$this->assertSame( $expected_id, $this->assertQuery( "SHOW TABLE STATUS LIKE 't'" )[0]->Auto_increment );
+			$this->assertSame(
+				$expected_id,
+				$this->assertQuery( "SELECT `AUTO_INCREMENT` FROM information_schema.tables WHERE table_name = 't'" )[0]->AUTO_INCREMENT
+			);
+		}
+
+		$this->assertQuery( "INSERT INTO t (name) VALUES ('next')" );
+		$this->assertSame( $expected_id, $this->assertQuery( "SELECT id FROM t WHERE name = 'next'" )[0]->id );
+	}
+
+	public static function tableRebuildsWithAutoIncrement(): array {
+		$states = array(
+			'deleted highest ID' => array(
+				array( "INSERT INTO t (name) VALUES ('a'), ('b'), ('c')", 'DELETE FROM t WHERE id = 3' ),
+				'4',
+			),
+			'deleted all rows'   => array(
+				array( "INSERT INTO t (name) VALUES ('a'), ('b'), ('c')", 'DELETE FROM t' ),
+				'4',
+			),
+			'empty with seed'    => array( array( 'ALTER TABLE t AUTO_INCREMENT = 1000' ), '1000' ),
+			'empty without seed' => array( array(), '1' ),
+			'large sequence'     => array(
+				array( "INSERT INTO t (id, name) VALUES (9007199254740993, 'a')", 'DELETE FROM t' ),
+				'9007199254740994',
+			),
+			'updated highest ID' => array(
+				array( "INSERT INTO t (name) VALUES ('a')", 'UPDATE t SET id = 100' ),
+				'101',
+			),
+		);
+		$cases  = array();
+		foreach ( array( '', 'TEMPORARY' ) as $temporary ) {
+			foreach ( array( 'ALTER TABLE t ADD COLUMN note TEXT', 'ALTER TABLE t MODIFY COLUMN name VARCHAR(100)', 'OPTIMIZE TABLE t', 'REPAIR TABLE t' ) as $rebuild ) {
+				foreach ( $states as $state => list( $setup, $expected_id ) ) {
+					$cases[ "$temporary $rebuild: $state" ] = array( $temporary, $rebuild, $setup, $expected_id );
+				}
+			}
+		}
+		return $cases;
+	}
+
+	public function testTableRebuildPreservesCreateTableAutoIncrementOption(): void {
+		$this->assertQuery( 'CREATE TABLE t (id INT AUTO_INCREMENT PRIMARY KEY, name TEXT) AUTO_INCREMENT = 1000' );
+		$this->assertQuery( 'ALTER TABLE t ADD COLUMN note TEXT' );
+		$this->assertQuery( 'OPTIMIZE TABLE t' );
+		$this->assertQuery( "INSERT INTO t (name) VALUES ('next')" );
+		$this->assertSame( '1000', $this->assertQuery( 'SELECT id FROM t' )[0]->id );
+	}
+
+	public function testTableRebuildAppliesExplicitAutoIncrementOption(): void {
+		$this->assertQuery( 'CREATE TABLE t (id INT AUTO_INCREMENT PRIMARY KEY, name TEXT) AUTO_INCREMENT = 1000' );
+		$this->assertQuery( 'ALTER TABLE t ADD COLUMN a INT, AUTO_INCREMENT = 500' );
+		$this->assertQuery( "INSERT INTO t (name) VALUES ('a')" );
+		$this->assertSame( '500', $this->assertQuery( "SELECT id FROM t WHERE name = 'a'" )[0]->id );
+
+		$this->assertQuery( 'ALTER TABLE t ADD COLUMN b INT, AUTO_INCREMENT = 1' );
+		$this->assertQuery( "INSERT INTO t (name) VALUES ('b')" );
+		$this->assertSame( '501', $this->assertQuery( "SELECT id FROM t WHERE name = 'b'" )[0]->id );
+
+		$this->assertQuery( 'ALTER TABLE t ADD COLUMN c INT, AUTO_INCREMENT = 2000' );
+		$this->assertQuery( "INSERT INTO t (name) VALUES ('c')" );
+		$this->assertSame( '2000', $this->assertQuery( "SELECT id FROM t WHERE name = 'c'" )[0]->id );
+	}
+
+	public function testTableRebuildPreservesAutoIncrementWithQuotedNames(): void {
+		$this->assertQuery( "CREATE TABLE `a``b'c` (`i``d` INT AUTO_INCREMENT PRIMARY KEY, name TEXT) AUTO_INCREMENT = 1000" );
+		$this->assertQuery( "ALTER TABLE `a``b'c` CHANGE COLUMN `i``d` `new``id` BIGINT AUTO_INCREMENT" );
+		$this->assertQuery( "INSERT INTO `a``b'c` (name) VALUES ('next')" );
+		$this->assertSame( '1000', $this->assertQuery( "SELECT `new``id` AS id FROM `a``b'c`" )[0]->id );
+	}
+
+	public function testTableRebuildPreservesAutoIncrementWithDifferentTableNameCase(): void {
+		$this->assertQuery( 'CREATE TABLE t (id INT AUTO_INCREMENT PRIMARY KEY, name TEXT) AUTO_INCREMENT = 1000' );
+		$this->assertQuery( 'ALTER TABLE T ADD COLUMN note TEXT' );
+		$this->assertQuery( "INSERT INTO t (name) VALUES ('next')" );
+		$this->assertSame( '1000', $this->assertQuery( 'SELECT id FROM t' )[0]->id );
+	}
+
+	public function testTableRebuildKeepsTemporaryAndPersistentSequencesSeparate(): void {
+		$this->assertQuery( 'CREATE TABLE t (id INT AUTO_INCREMENT PRIMARY KEY, name TEXT) AUTO_INCREMENT = 1000' );
+		$this->assertQuery( 'CREATE TEMPORARY TABLE t (id INT AUTO_INCREMENT PRIMARY KEY, name TEXT) AUTO_INCREMENT = 500' );
+		$this->assertQuery( 'ALTER TABLE t ADD COLUMN note TEXT' );
+		$this->assertQuery( 'OPTIMIZE TABLE t' );
+		$this->assertQuery( "INSERT INTO t (name) VALUES ('temporary')" );
+		$this->assertSame( '500', $this->assertQuery( 'SELECT id FROM t' )[0]->id );
+
+		$this->assertQuery( 'DROP TEMPORARY TABLE t' );
+		$this->assertQuery( 'ALTER TABLE t ADD COLUMN note TEXT' );
+		$this->assertQuery( "INSERT INTO t (name) VALUES ('persistent')" );
+		$this->assertSame( '1000', $this->assertQuery( 'SELECT id FROM t' )[0]->id );
+	}
+
+	public function testTableRebuildWithoutAutoIncrement(): void {
+		$this->assertQuery( 'CREATE TABLE t (id INT PRIMARY KEY, name TEXT)' );
+		$this->assertQuery( "INSERT INTO t VALUES (1, 'a')" );
+		$this->assertQuery( 'ALTER TABLE t ADD COLUMN note TEXT' );
+		$this->assertQuery( 'OPTIMIZE TABLE t' );
+		$this->assertSame( 'a', $this->assertQuery( 'SELECT name FROM t' )[0]->name );
+		$this->assertFalse( $this->sqlite->query( "SELECT 1 FROM sqlite_master WHERE name = 'sqlite_sequence'" )->fetchColumn() );
+
+		$this->assertQuery( 'ALTER TABLE t MODIFY COLUMN id INT AUTO_INCREMENT' );
+		$this->assertQuery( "INSERT INTO t (name) VALUES ('b')" );
+		$this->assertSame( '2', $this->assertQuery( "SELECT id FROM t WHERE name = 'b'" )[0]->id );
+
+		$this->assertQuery( 'ALTER TABLE t AUTO_INCREMENT = 1000' );
+		$this->assertQuery( 'ALTER TABLE t MODIFY COLUMN id INT NOT NULL' );
+		$this->assertFalse( $this->sqlite->query( "SELECT seq FROM sqlite_sequence WHERE name = 't'" )->fetchColumn() );
+		$this->assertSame( null, $this->assertQuery( "SHOW TABLE STATUS LIKE 't'" )[0]->Auto_increment );
+	}
+
+	public function testFailedTableRebuildPreservesAutoIncrement(): void {
+		$this->assertQuery( 'CREATE TABLE t (id INT AUTO_INCREMENT PRIMARY KEY, name TEXT)' );
+		$this->assertQuery( "INSERT INTO t (name) VALUES ('a'), ('a'), ('b')" );
+		$this->assertQuery( 'DELETE FROM t WHERE id = 3' );
+		try {
+			$this->assertQuery( 'ALTER TABLE t ADD UNIQUE KEY unique_name (name)' );
+			$this->fail( 'Adding a unique key on duplicate values must fail.' );
+		} catch ( WP_MySQL_On_SQLite_Exception $e ) {
+			$this->assertSame( '23000', $e->getCode() );
+		}
+		$this->assertQuery( "INSERT INTO t (name) VALUES ('next')" );
+		$this->assertSame( '4', $this->assertQuery( "SELECT id FROM t WHERE name = 'next'" )[0]->id );
+		$this->assertSame( array( 't' ), $this->sqlite->query( 'SELECT name FROM sqlite_sequence' )->fetchAll( PDO::FETCH_COLUMN ) );
+	}
+
 	public function testTemporaryTableAutoIncrement(): void {
 		// Persistent and temporary tables must keep independent sequences.
 
diff --git a/packages/mysql-on-sqlite/tests/WP_MySQL_On_SQLite_Tests.php b/packages/mysql-on-sqlite/tests/WP_MySQL_On_SQLite_Tests.php
index 64c9ad8c9..03a67acaa 100644
--- a/packages/mysql-on-sqlite/tests/WP_MySQL_On_SQLite_Tests.php
+++ b/packages/mysql-on-sqlite/tests/WP_MySQL_On_SQLite_Tests.php
@@ -6753,6 +6753,24 @@ public function testConfigurationNormalizesStoredTemporalZeroDefaults(): void {
 		$this->assertEquals( $expected_rows, $this->last_result );
 	}
 
+	public function testConfigurationPreservesAutoIncrementWhenNormalizingTemporalZeroDefaults(): void {
+		$this->assertQuery( 'CREATE TABLE _tmp_table (id INT AUTO_INCREMENT PRIMARY KEY, created_at DATETIME NOT NULL DEFAULT 0)' );
+		$this->assertQuery( 'CREATE TABLE _tmp_empty (id INT AUTO_INCREMENT PRIMARY KEY, created_at DATETIME NOT NULL DEFAULT 0)' );
+		$this->sqlite->exec( "UPDATE _wp_sqlite_mysql_information_schema_columns SET column_default = '0' WHERE table_name IN ('_tmp_table', '_tmp_empty') AND column_name = 'created_at'" );
+		$this->assertQuery( 'OPTIMIZE TABLE _tmp_table, _tmp_empty' );
+		$this->assertQuery( 'INSERT INTO _tmp_table (id) VALUES (1), (2), (3)' );
+		$this->assertQuery( 'DELETE FROM _tmp_table WHERE id = 3' );
+		$this->assertQuery( 'ALTER TABLE _tmp_empty AUTO_INCREMENT = 1000' );
+
+		$this->reconnectAfterDriverUpgrade();
+
+		$this->assertQuery( 'INSERT INTO _tmp_table (id) VALUES (NULL)' );
+		$this->assertSame( '4', $this->assertQuery( 'SELECT MAX(id) AS id FROM _tmp_table' )[0]->id );
+		$this->assertQuery( 'INSERT INTO _tmp_empty (id) VALUES (NULL)' );
+		$this->assertSame( '1000', $this->assertQuery( 'SELECT id FROM _tmp_empty' )[0]->id );
+		$this->assertSame( '0000-00-00 00:00:00', $this->assertQuery( 'SELECT created_at FROM _tmp_empty' )[0]->created_at );
+	}
+
 	public function testConfigurationNormalizesStoredTemporalZeroValuesWithoutRunningTriggers(): void {
 		$this->assertQuery(
 			'CREATE TABLE _tmp_table (
diff --git a/packages/mysql-on-sqlite/tests/WP_MySQL_On_SQLite_Translation_Tests.php b/packages/mysql-on-sqlite/tests/WP_MySQL_On_SQLite_Translation_Tests.php
index a09a0dcdb..26b29efcd 100644
--- a/packages/mysql-on-sqlite/tests/WP_MySQL_On_SQLite_Translation_Tests.php
+++ b/packages/mysql-on-sqlite/tests/WP_MySQL_On_SQLite_Translation_Tests.php
@@ -896,6 +896,7 @@ public function testAlterTableAddColumn( bool $stringify_fetches ): void {
 				'PRAGMA foreign_keys = OFF',
 				'CREATE TABLE `<tmp-table>` ( `id` INTEGER, `a` INTEGER )' . $this->strict_suffix,
 				'INSERT INTO `<tmp-table>` (`rowid`, `id`) SELECT `rowid`, `id` FROM `t`',
+				"SELECT 1 FROM main.sqlite_master WHERE type = 'table' AND name = 'sqlite_sequence'",
 				'DROP TABLE `t`',
 				'ALTER TABLE `<tmp-table>` RENAME TO `t`',
 				'PRAGMA foreign_key_check',
@@ -934,6 +935,7 @@ public function testAlterTableAddColumnWithNotNull(): void {
 				'PRAGMA foreign_keys = OFF',
 				'CREATE TABLE `<tmp-table>` ( `id` INTEGER, `a` INTEGER NOT NULL )' . $this->strict_suffix,
 				'INSERT INTO `<tmp-table>` (`rowid`, `id`) SELECT `rowid`, `id` FROM `t`',
+				"SELECT 1 FROM main.sqlite_master WHERE type = 'table' AND name = 'sqlite_sequence'",
 				'DROP TABLE `t`',
 				'ALTER TABLE `<tmp-table>` RENAME TO `t`',
 				'PRAGMA foreign_key_check',
@@ -965,6 +967,7 @@ public function testAlterTableAddColumnWithDefault(): void {
 				'PRAGMA foreign_keys = OFF',
 				'CREATE TABLE `<tmp-table>` ( `id` INTEGER, `a` INTEGER DEFAULT \'0\' )' . $this->strict_suffix,
 				'INSERT INTO `<tmp-table>` (`rowid`, `id`) SELECT `rowid`, `id` FROM `t`',
+				"SELECT 1 FROM main.sqlite_master WHERE type = 'table' AND name = 'sqlite_sequence'",
 				'DROP TABLE `t`',
 				'ALTER TABLE `<tmp-table>` RENAME TO `t`',
 				'PRAGMA foreign_key_check',
@@ -996,6 +999,7 @@ public function testAlterTableAddColumnWithNotNullAndDefault(): void {
 				'PRAGMA foreign_keys = OFF',
 				'CREATE TABLE `<tmp-table>` ( `id` INTEGER, `a` INTEGER NOT NULL DEFAULT \'0\' )' . $this->strict_suffix,
 				'INSERT INTO `<tmp-table>` (`rowid`, `id`) SELECT `rowid`, `id` FROM `t`',
+				"SELECT 1 FROM main.sqlite_master WHERE type = 'table' AND name = 'sqlite_sequence'",
 				'DROP TABLE `t`',
 				'ALTER TABLE `<tmp-table>` RENAME TO `t`',
 				'PRAGMA foreign_key_check',
@@ -1027,6 +1031,7 @@ public function testAlterTableAddMultipleColumns(): void {
 				'PRAGMA foreign_keys = OFF',
 				'CREATE TABLE `<tmp-table>` ( `id` INTEGER, `a` INTEGER, `b` TEXT COLLATE NOCASE, `c` INTEGER )' . $this->strict_suffix,
 				'INSERT INTO `<tmp-table>` (`rowid`, `id`) SELECT `rowid`, `id` FROM `t`',
+				"SELECT 1 FROM main.sqlite_master WHERE type = 'table' AND name = 'sqlite_sequence'",
 				'DROP TABLE `t`',
 				'ALTER TABLE `<tmp-table>` RENAME TO `t`',
 				'PRAGMA foreign_key_check',
@@ -1064,6 +1069,7 @@ public function testAlterTableDropColumn(): void {
 				'PRAGMA foreign_keys = OFF',
 				'CREATE TABLE `<tmp-table>` ( `id` INTEGER )' . $this->strict_suffix,
 				'INSERT INTO `<tmp-table>` (`rowid`, `id`) SELECT `rowid`, `id` FROM `t`',
+				"SELECT 1 FROM main.sqlite_master WHERE type = 'table' AND name = 'sqlite_sequence'",
 				'DROP TABLE `t`',
 				'ALTER TABLE `<tmp-table>` RENAME TO `t`',
 				'PRAGMA foreign_key_check',
@@ -1096,6 +1102,7 @@ public function testAlterTableDropMultipleColumns(): void {
 				'PRAGMA foreign_keys = OFF',
 				'CREATE TABLE `<tmp-table>` ( `id` INTEGER )' . $this->strict_suffix,
 				'INSERT INTO `<tmp-table>` (`rowid`, `id`) SELECT `rowid`, `id` FROM `t`',
+				"SELECT 1 FROM main.sqlite_master WHERE type = 'table' AND name = 'sqlite_sequence'",
 				'DROP TABLE `t`',
 				'ALTER TABLE `<tmp-table>` RENAME TO `t`',
 				'PRAGMA foreign_key_check',
@@ -1134,6 +1141,7 @@ public function testAlterTableAddAndDropColumns(): void {
 				'PRAGMA foreign_keys = OFF',
 				'CREATE TABLE `<tmp-table>` ( `b` INTEGER )' . $this->strict_suffix,
 				'INSERT INTO `<tmp-table>` (`rowid`) SELECT `rowid` FROM `t`',
+				"SELECT 1 FROM main.sqlite_master WHERE type = 'table' AND name = 'sqlite_sequence'",
 				'DROP TABLE `t`',
 				'ALTER TABLE `<tmp-table>` RENAME TO `t`',
 				'PRAGMA foreign_key_check',
@@ -1170,6 +1178,7 @@ public function testAlterTableDropAndAddSingleColumn(): void {
 				'PRAGMA foreign_keys = OFF',
 				'CREATE TABLE `<tmp-table>` ( `a` INTEGER )' . $this->strict_suffix,
 				'INSERT INTO `<tmp-table>` (`rowid`) SELECT `rowid` FROM `t`',
+				"SELECT 1 FROM main.sqlite_master WHERE type = 'table' AND name = 'sqlite_sequence'",
 				'DROP TABLE `t`',
 				'ALTER TABLE `<tmp-table>` RENAME TO `t`',
 				'PRAGMA foreign_key_check',