In 1851, Ingres, at 71 years of age, gave part of his collection, including copies, work of pupils, and Greek vases, as a gift to the city of his birth. The Ingres room was inaugurated in 1854. The death of Ingres in January 1867 led to a considerable enrichment of the collection with additional works, in particular several thousands of drawings.
The museum is located in a building that once served as the residence of the bishops of Montauban. The structure belongs chiefly to the 17th century, but some portions are much older, notably an underground chamber known as the Hall of the Black Prince (Salle du Prince Noir). During World War II, the Musée Ingres served as one of the temporary places of storage for the Mona Lisa, evacuated from the Louvre at the beginning of the war. A renovation carried out between 1951–1958 made Musée Ingres a modern institution according to the designs of the time, equipped with additional inventories.
Among the paintings by Ingres in the collection are the following: