In 642, Umar appointed al-Mughira governor of Kufa, the other Arab garrison town of Iraq. Two years later, a former slave of al-Mughira, known as Abu Lu'lu'a, assassinated Umar while the latter was praying in Medina. Umar's successor, Caliph Uthman (), kept al-Mughira as governor for another year until replacing him with Sa'd ibn Abi Waqqas. Al-Mughira retired from public life and returned to Ta'if upon the accession of Caliph Ali () following Uthman's assassination in 656. From his hometown, he observed the chaotic events of the First Muslim Civil War between the supporters of Ali, who made Kufa his capital, and the bulk of the Quraysh, who opposed Ali's caliphate. When Ali and Mu'awiya ibn Abi Sufyan, the governor of Syria who had taken up the cause of avenging the death of his Umayyad kinsman Uthman, decided to settle the Battle of Siffin by arbitration in 657, al-Mughira, without invitation by either side, attended the talks at Adhruh.