Incorporated in 1948, the museum's original home was a three-room building on Charlotte Street, once the land sales office of
E.W. Grove, developer of the
Grove Park Inn. By 1950, the museum began acquiring a permanent collection. Quickly, the collection outgrew its home, and the museum moved to donated space on the 15th floor of the Northwestern Bank Building, now
the Arras Building. Forced to move out of the donated bank building space, the museum purchased property at 152 Pearson Drive (the Gay Green House) in the
Montford Area Historic District of Asheville, and exhibitions became more regional in scope. Programming and attendance expanded, but the aging 40-year-old building presented problems. When plans for the
Asheville Civic Center were announced in 1972, the museum board accepted an invitation to be one of the three cultural agencies in the center. In 1976, the museum opened a facility in the Civic Center. In 1984, the Asheville Art Museum became one of few of its size to be accredited by the
American Alliance of Museums. In 1992, the museum opened in a 1925
Italian Renaissance style building with contemporary additions that once housed
Pack Memorial Library. That facility includes of space in the Pack Place Education, Arts & Science Center complex in downtown Asheville. A modest capital expansion, completed in 1999, added space from Pack Place and the adjacent Legal Building, creating new classroom and studio facilities, an art library, a teacher resource center, a community gallery and a new entrance. Following this expansion, the museum occupied of space. Between September 2016 and November 2019, the museum expanded into space formerly occupied by The Health Adventure, increasing its size to 54,000 square feet. During this expansion, the permanent collection grew to comprise 8,000+ works (a 31.5% increase since 2017). The museum reopened on November 14, 2019. The first public art installation in the plaza is the six-foot diameter chiseled glass orb entitled "Reflections on Unity" by the artist
Henry Richardson. In June 2022 the Asheville Art Museum was one of three museums to be awarded the 2022 National Medal for Museum and Library Service by the
Institute of Museum and Library Services. == Leadership ==