The Missoula Art Museum began its collection in 1973 with the Missoula Festival of the Arts exhibition purchase awards that were given to Gennie DeWeese, Walter Hook, and Jessie Wilber. The Festival was able to raise the fund needed to establish the Museum, which opened in 1975 as county-run museum.

With a steady growth for the past 20 years in terms of programming and collecting, the Museum became an independent non-profit entity called the Art Museum of Missoula. It continued to expand. It eventually changed its name to Missoula Art Museum.

Its collection boasts of more than 700 artworks that have been acquired by the Museum since 1995. Among these is the Contemporary American Indian Art Collection featuring more than 110 works. It is one of the biggest bodies of contemporary Native art in the county.