Formerly known as Anao, the site of Saint-Jean-Cap-Ferrat was initially occupied by the Ligurians, then by the Lombards around 575. In the early Middle Ages, the recluse Saint Hospice occupied a tower on the eastern part of the peninsula. In the 8th century, the Saracens conquered the site; they were not dislodged until the 11th century.

In 1388, when the county of Nice surrendered, the hamlet of Saint-Jean, which was part of the commune of Villefranche, returned to the duchy of Savoy. The site was fortified under the Savoyard protectorate; in 1561, under the reign of Duke Emmanuel-Philibert of Savoy, the Saint-Hospice fort was built. It was taken and destroyed in 1706 by the Duke of Berwick, when Nice was taken by France.

Saint-Jean passed several times under French occupation between 1720 and 1820; it was definitively attached to France in 1860 with the whole of the county of Nice.

In 1904, the hamlet of Saint-Jean-sur-Mer became an independent village from Villefranche-sur-Mer and was renamed Saint-Jean-Cap-Ferrat in 1907.

Today, the area is one of the main residential sites on the Côte d'Azur, with many luxurious properties.