The Painting Gallery (1965) building is built underground with an entrance modeled on Agamemnon's Tomb in Mycenae, Greece. Paintings are displayed on a system of three revolving racks of carpeted panels. Johnson and Whitney acquired a large collection over the course of 40 years, but much of it was sold to support the trust after Johnson's death. The gallery still includes a portrait of Johnson by Andy Warhol as well as works by Frank Stella, Jasper Johns, Julian Schnabel and Robert Rauschenberg. Julian Schnabel also did the brass sculpture resembling petrified wood adjacent to the Sculpture Gallery.
The Sculpture Gallery (1970) is a modernist design featuring a glass and steel girder ceiling that projects zebra-like dappled sunlight. A Frank Stella sculpture is shown.