One of his earliest known paintings is the large panel portrait of King Charles VII, painted around 1445. The painting is believed to have been produced before Fouquet’s trip to Rome as there is no evidence of Italian influence. The portrait is abstractly staged and objective.
In 1446, he travelled to Rome as a part of a French mission. There he painted Pope Eugenius IV with his two nephews. This portrait caused quite a sensation as it was painted on canvas rather than on the more common wood support.
While in Rome he gained a first-hand experience of Italian Renaissance and studied the works of painters like Masaccio, Fra Angelico and Piero della Francesca. Italian art had a profound impact on his future painting style. After he returned to France, he opened a workshop in Tours.
His workshop proved to be quite successful and he received commissions from French nobility. King Charles VII was one of his regular patrons who greatly admired his art.
Around 1450 he made a self-portrait which featured a small, painted enamel roundel which was unusual for his time. It is also likely to be the earliest sole self-portrait surviving in Western art.
He possessed considerable expertise as an illuminator. He was very precise in rendering the finest of details, and his proficiency in creating the minutest of illustrations earned him the reputation of being a manuscript illuminator par excellence.
In the early 1450s, Fouquet started working on the ‘Melun Diptych’, which would become his most famous work. The right panel of the painting shows the Virgin and Child, surrounded by angels. The painting caused considerable controversy as the Virgin is a recognizable portrait of Agnes Sorel, the King's mistress, shown with an exposed breast.
Between 1450 and 1460, he produced several works for the royal secretary and lord treasurer, Étienne Chevalier. One of the major works he created was a large ‘Book of Hours’ with about 60 full-page miniatures.
During this time, he also worked on two richly illuminated manuscripts of a French translation of Boccaccio’s ‘De casibus virorum illustrium’ (‘On the Fates of Famous Men’) and ‘De claris mulieribus’ (‘On Famous Women’). He also made his only monumental painting, the large altarpiece of the “Pietà” in the church at Nouans in this period.
When King Charles VII died in 1461, Jean Fouquet was commissioned to make a colored death mask for the King's public funeral. Fouquet enjoyed even more prominence in the administration of Charles’ successor King Louis XI.
King Louis XI founded the Order of St. Michael in 1469, and commissioned Fouquet to illuminate the statutes of the order. The King was much impressed by his works and appointed him the peintre du roy (Court Painter) in 1475.
As the Court Painter, he enjoyed unprecedented success. In this position he supervised a large workshop that produced paintings and manuscripts. Over the course of his career, he also worked on assignments like painting banners and painting a canopy for the ceremonial entrance of Alfonso V of Portugal into Tours.