Founded in 1959 and now comprising four wings, more than 6,000 works, and more than 28,000 square feet of exhibition space, the Colby College Museum of Art has built a significant permanent collection that specializes in American and contemporary art. The museum serves as a teaching resource for Colby and as an active cultural institution for residents of Maine and visitors to the state.

In the early 1950s Adeline and Caroline Wing gave important paintings by William Merritt Chase, Winslow Homer, and others. In 1956 Ellerton M. and Edith Jetté donated their American Heritage Collection, consisting of 76 works by American folk artists. The next year the Helen Warren and Willard Howe Cummings Collection of American paintings and watercolors was given.

In 1973 the Jetté Galleries were added to the Bixler Art and Music Center. That year Norma B. Marin and John Marin Jr. gave 25 works of art by John Marin. Through the Marins' continued generosity, the John Marin Collection at the Colby College Museum of Art has become the largest collection of Marin's work in any academic museum in the world.

Though the majority of the museum’s works are American, excellent examples of European prints, drawings, and paintings and special collections such as the Bernat Collection of Oriental Ceramics are integral to the museum’s holdings. The collection’s growth is assured in part by the bequest of Jere Abbott, the first associate director of the Museum of Modern Art, who established a significant acquisition endowment, enabling Colby to purchase major works by artists such as Robert Henri, Paul Manship, Robert Rauschenberg, Agnes Martin, Kara Walker, and Hiroshi Sugimoto.

In 1992 the museum received a gift of 414 works by Alex Katz from the artist, and in 1996 a wing comprising more than 8,000 square feet was constructed to house this collection. The Paul J. Schupf Wing for the Works of Alex Katz was made possible through the generosity of Colby benefactor Paul J. Schupf. Through rotating exhibitions it showcases a diverse collection of the artist's work across media, and it is one of only a handful of museum wings dedicated to the work of a living artist. The museum holds nearly 700 works by Alex Katz.

With a lead gift from Peter and Paula Lunder, important benefactors of the College, a new wing opened in 1999 for the exhibition of Colby's renowned collection of American art. The Lunder Wing was designed by architect Frederick Fisher, one of the world's leading designers of museum spaces, and it comprises 13 galleries and 9,000 square feet of exhibition space.

In recent years site-specific sculptures by Richard Serra and Sol LeWitt have been installed in outdoor spaces adjacent to the museum. In 2004, through a partial gift of the artist and Universal Limited Art Editions (ULAE), the museum became the sole repository of the complete print oeuvre of Terry Winters. In 2006 Paul J. Schupf promised the museum his collection of more than 150 prints and drawings by Richard Serra, making Colby one of the largest repositories of Serra’s works on paper. Recent gifts from the Alex Katz Foundation also have had great impact on the contemporary collection, and they include important works by Adolph Gottlieb, Rudy Burckhardt, Chuck Close, Jennifer Bartlett, Elizabeth Murray, and others.

In 2007 Peter and Paula Lunder promised their collection of more than 500 works of art to the museum. This gift constitutes one of the most important art collections ever donated to a liberal arts college. Significant works of 19th- and 20th-century American art, including more than 200 prints by James McNeill Whistler, make up this extraordinary gift.