Founded by Anna and August Heckscher in 1920, the museum was based on his initial donation of 185 works of art.

The oldest major work is Lucas Cranach the Elder's Virgin, Child, St. John the Baptist and Angels of 1534.

The modern and abstract art collections are extensive and includes artists such as Ilya Bolotowsky, Georgia O'Keeffe, Knox Martin, and Esphyr Slobodkina.

The museum also features many works from one-time Huntington residents such as Arthur Dove, Helen Torr, and George Grosz.

The photography collection features the work of Berenice Abbott, Larry Fink, Eadweard Muybridge, and Man Ray's Electricité portfolio of 1931.