He was the second son of John II of Montferrat and Isabella of Majorca and brother and successor of Secondotto.
On 3 January 1379, John III was installed as margrave under the regency of his uncle Otto, Duke of Brunswick-Grubenhagen.
Desirous of avenging his brother's death and recuperating the territory lost in the aftermath of Secondotto's retreat, John declared war on the Visconti of Milan, but was forced to sign a peace before fighting had begun, under the pressure of the Antipope Clement VII of Avignon, who wished to have Otto of Brunswick at his court.
In order to guarantee the survival of the margraviate, Otto placed it under the protection of the Kingdom of France.
On 25 August 1381, they were involved in a battle in which Otto was captured and the young John slain.