MNA co-founder Harold S. Colton designed the museum building and considered it his magnum opus. Built during the Depression with local malpais (lava rock) masonry, the building opened in the spring of 1936. The move from the original quarters at the Flagstaff Women’s Club enabled exhibits and collections to be under one roof. The original structure included the south entrance, the anthropology and geology galleries, the bookstore, and museum shop.
The first exhibits included a loggia for special exhibits, the geology and anthropology galleries, and two rooms for the anthropology and natural history study collections. Additions through the years include work and office areas, a photographic studio, patio, the ethnology wings, and the Museum Shop.
The flagpole and lookout near the entrance were built in 1950. The nature trail was created in 1956 and the cinder walk to the main entrance was laid with flagstone in 1967. The building was added to the National Register of Historic Places in 1993.
The Branigar/Chase Discovery Center was the newest addition to the museum building, featuring an auditorium with bleacher seating, a fine arts gallery, multipurpose rooms, dressing rooms, a kitchen, courtyard and outdoor activity area, and upstairs offices. The reception area features replicated details of the Historic Colton House, including the fireplace and living room with its mission-style furniture. The building opened in the summer of 1995 and is named for the Harvey C. Branigar and the David K. Chase families.