Following the death of his brother Olivier in 1433, John succeeded to his family's hereditary titles in Brittany, including the family's claim to the Breton ducal throne. In 1437, he also purchased the county of Périgord from Charles, Duke of Orléans. He only entered into possession of his Breton lands in 1448 after reconciling with Francis I, Duke of Brittany. During the final campaigns of the Hundred Years’ War, he served as lieutenant general for Charles VII of France in Aquitaine between 1450 and 1451 and he distinguished himself at the Battle of Castillon in 1453.