Following the death of Muhammad in 632, leadership of the emergent Muslim state passed to Abu Bakr, who retained al-Mughira in an administrative capacity. During this period, most high-ranking government posts were reserved for members of the Quraysh, the tribe of both Muhammad and the Caliph. Al-Mughira continued his military service and lost an eye during the
Battle of the Yarmuk in August 636. Caliph
Umar () appointed him governor of
Basra, , a newly founded garrison town that served as the primary springboard for the
Muslim conquest of Persia. However, his tenure there was cut short when he was dismissed following allegations of adultery. In 642, Umar reappointed al-Mughira as the governor of Kufa, the other major Arab garrison town in Iraq, where he succeeded Ammar ibn Yasir. Two years into this second governorship, a former slave of al-Mughira known as Abu Lu'lu'a assassinated Caliph Umar while he 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
Udhruh. == Death ==