The Museum of Art, housed in the Bixler art and music complex, boasts a significant permanent collection of drawings and paintings highlighted by a large group of works by Alex Katz, Winslow Homer, and John Marin. The Jette and Davis galleries house Colby's extensive collection of American and European artists. The museum alternates selections from the permanent collection with temporary loan exhibitions, including the Joan Whitney Payson Collection of Impressionist and Post-Impressionist Art every other spring semester. The Paul Schupf Wing for the Art of Alex Katz, completed in 1996, makes the Colby museum one of the few in the United States with a wing devoted solely to the work of a living artist. Katz, who has summered in Maine since the 1950s, donated more than 400 of his works to the museum with the understanding that a wing would be built especially for showing his large, signature paintings.

The museum is normally open from 10 a.m. to 4:30 p.m., Monday through Saturday, and from 2 p.m. to 4:30 p.m. on Sunday.