The first ducal castle was built in the 13th century on top of the (still visible) Gallo-Roman wall of the town, where the Namnetes settled. It was demolished in the 15th century to make way for the present building.
The current castle was the work of Francis II, the last Duke of an independent Brittany, who wanted to make the Château des ducs de Bretagne both a military fortress, which could act as a defence against the King, and the principal residence of the ducal court. Work was continued by Duchess Anne of Brittany, twice Queen of France through her marriages to Charles VIII and Louis XII. Her influence can be seen in the sculptural décor (dormer windows overlooking the main residence, as well as the coat of arms and loggias on the “Golden Crown” tower), marked by the first signs of the Italian Renaissance.
Following the integration of Brittany into France in 1532, during the 16th and 17th centuries, the Château des ducs de Bretagne became the residence of the kings of France when they visited Brittany, and later a military barracks, an arsenal, and a prison. For three centuries, it endured countless transformations and considerable damage: fortifications, a fire in 1670, construction of the Military Saddlery (Bâtiment du Harnachement) for storing artillery equipment, an explosion in 1800, and so on.
Listed as a historical monument in 1862, it was sold by the government to the City of Nantes in 1915 before also becoming, in 1924, a municipal museum. During World War II, the occupying German forces built a bunker there.