Local artists started the museum in 1948 - painters and printmakers who wanted a permanent venue in a city that already had a serious creative scene. The first paid director, James Neumann, arrived in 1965 just as the museum moved from Charlotte Street to the Northwestern Bank Building. Through the late 1960s and 1970s the museum changed addresses repeatedly: the Montford District, then back downtown. Ed Ritts, who served as director from 1980 to 1995, won the museum's American Alliance accreditation, broadened its acquisitions beyond regional artists, and engineered the move to Pack Place in the early 1990s. Pamela Myers has run the institution since December 1995 - one of the longest tenures of any American museum director.

Twenty miles east of downtown, between 1933 and 1957, Black Mountain College ran an experimental program that attracted Josef and Anni Albers, John Cage, Merce Cunningham, Willem and Elaine de Kooning, Buckminster Fuller, Robert Rauschenberg, Cy Twombly, and dozens more. The college closed. The artists scattered. But Asheville stayed close to the work. The Asheville Art Museum holds one of the country's most significant collections of Black Mountain College art - paintings, prints, textiles, and the documentary photography that captured the place before it dissolved. The Black Mountain College Museum + Arts Center, a separate institution down the street, runs its own programs. Between the two, the legacy of those twenty-four mountain summers stays alive in a city the college only sometimes visited.

Western North Carolina has been a studio craft heartland since the Penland School of Craft and the John C. Campbell Folk School began training potters, weavers, blacksmiths, and woodworkers earlier in the twentieth century. The museum collects this work - not as folk curiosity, but as serious contemporary practice. Cherokee artists from the Qualla Boundary, the Eastern Band's land just west of here, are also part of the permanent collection. Basketry, pottery, jewelry, painting, sculpture - work that ranges from traditional doublewoven river-cane baskets to contemporary mixed-media pieces. The combination is unusual: a museum where Bauhaus refugees, Appalachian potters, and Cherokee artists share gallery walls.

The Asheville Art Museum closed in September 2016 to expand into the space formerly occupied by The Health Adventure, an interactive science center that had shared the Pack Place complex. The renovation took three years and $24 million. When the doors reopened on November 14, 2019, the permanent collection had grown 31.5%. The new space included expanded exhibition galleries, an art education facility, a rooftop sculpture terrace, and visible storage windows letting the public see normally-archived work. In June 2022 the museum received the National Medal for Museum and Library Service - the highest federal honor for American museums, given to only three institutions that year.

The museum sits at 2 South Pack Square in the center of downtown Asheville. The square itself is named for George Willis Pack, a lumberman-philanthropist who in 1901 gave the land for a public space and library. Today the museum, the courthouse, the city hall, and the Vance Monument cluster around the same plaza - a compact civic center that lets visitors walk between art, government, and history in under five minutes. The orb in the courtyard, the brick of the old Pack Library, the Art Deco curves of the city hall a block away - they belong to the same conversation about what a small mountain city wants to be.