Jean was the natural son of Louis, Duke d'Orléans, by his liaison with Mariette d'Enghien. Jean entered the service of his cousin the dauphin, the future Charles VII, in 1420 and became his trusted adviser; he was later appointed grand chamberlain. His first notable success was the defeat of the English at Montargis (1427), and during 1427–28 he defended Orléans until Joan of Arc arrived. He then took part in the Battle of Patay and accompanied Charles to Reims for his coronation. He captured Chartres and Lagny in 1432 and engaged in a series of campaigns culminating in a triumphal entry into Paris in 1436.

He shared in the negotiations with the English at Gravelines (1439) and worked with Charles on the reorganization of the military. He received the countship of Dunois from his half brother, Charles, Duke d'Orléans, and later received the countship of Longueville (1443) from Charles VII. He helped negotiate the truce of 1444 with the English and in 1447–49 the abdication of the antipope Felix V. At the end of the truce, he served in the reconquest of Normandy (1449–50) and Guyenne (1451). Charles VII later entrusted him with the arrest of the Duke d'Alençon (Jean II) in 1456 and with measures against the intrigues of the dauphin, the future Louis XI. When Louis acceded to the throne, Dunois joined the League of the Public Weal against him, but he made his peace with him and returned to royal service. The future dukes de Longueville descended from his marriage to Marie d'Harcourt.