In 1930 Mexican muralist Diego Rivera was hired to paint The Making of a Fresco Showing the Building of a City, which is located in the student-directed art gallery.

During its first 60 years, influential artists associated with the school included Eadweard Muybridge, photographer and pioneer of motion graphics; Maynard Dixon, painter of San Francisco's labor movement and of the landscape of the West; Henry Kiyama, whose Four Immigrants Manga was the first graphic novel published in the U.S.; Sargent Claude Johnson, one of the first African-American artists from California to achieve a national reputation; Louise Dahl-Wolfe, an innovative photographer whose work for Harper's Bazaar in the 1930s defined a new American style of "environmental" fashion photography; Gutzon Borglum, the creator of the large-scale public sculpture known as Mount Rushmore; Rudolf Hess, German Expressionist painter and art critic, Emily Carr, Modernist Canadian painter well known for her work with indigenous culture,[8] and numerous others.

After World War II ended (1945) the school became a nucleus for Abstract Expressionism, with faculty including Clyfford Still, Ad Reinhardt, Mark Rothko, David Park, Elmer Bischoff, and Clay Spohn.

In this spirit of advancement, in 1949 CSFA Director Douglas MacAgy organized an international conference, The Western Roundtable on Modern Art, which included Marcel Duchamp, Frank Lloyd Wright, and Gregory Bateson.

By the early 1950s, San Francisco's North Beach had become the West Coast center of the Beat Movement, and music, poetry, and discourse were an intrinsic part of artists' lives.

In 1953 he and his partner, poet Robert Duncan, along with painter Harry Jacobus, started the King Ubu Gallery, an important alternative space for art, poetry, and music.

Students in the early to mid-1960s included artists Ronald Davis, Robert Graham, Forrest Myers, Leo Valledor, Michael Heizer, Ronnie Landfield, Peter Reginato, Gary Stephan, and John Duff and in the late 1960s Annie Leibovitz, who would soon begin photographing for Rolling Stone magazine; Paul McCarthy, well known for his performance and sculpture works; and Charles Bigelow, who would be among the first typographers to design fonts for computers.

In 1969, a new addition to the building by Paffard Keatinge-Clay added 22,500 sq ft (2,090 m2) of studio space, a large theater/lecture hall, an outdoor amphitheater, galleries, and a cafe.

The faculty during this period included George Kuchar, Gunvor Nelson, Howard Fried, Paul Kos, Angela Davis, Kathy Acker, Robert Colescott, and many other influential artists and writers.

As students at SFAI, Barry McGee, Aaron Noble, and Rigo 23, among others, were part of the movement known as the Mission School, taking their graffiti-inspired art to the streets and walls of the city.

[13] Due to financial mismanagement, declining enrollment, high real estate costs, and a reliance on income from campus property rentals, which was affected by the COVID-19 pandemic,[14] the school announced on March 23, 2020, that it would stop accepting new students for the following fall semester.

[24] In late February 2024, a nonprofit corporation endowed by Laurene Powell Jobs bought the campus including the mural for approximately $30 million, with the stated intention of continuing its use as an arts institution, plus possible on-campus housing for artists in residence.

Throughout the SFAI Painting Department's history, it had been home to celebrated artists such as Clyfford Still, Mark Rothko, Richard Diebenkorn, Jay DeFeo, Fred Martin, Bruce McGaw, Elmer Bischoff, David Park, David Simpson, Frank Lobdell, Roy De Forest, Joan Brown, Ronald Davis, William T. Wiley, Toba Khedoori, Barry McGee, Inez Storer and Kehinde Wiley among others and was central to movements such as Abstract Expressionism, Bay Area Figuration, Color Field, California Funk, and the Mission School.

Among the many artist musicians who studied at SFAI are Jerry Garcia, guitarist in Grateful Dead; Dave Getz, drummer for Big Brother and the Holding Company and Country Joe and the Fish; Prairie Prince of The Tubes; Debora Iyall of Romeo Void; Freddy (aka Fritz) of the Mutants; Penelope Houston of the Avengers, Courtney Love, actress and rock musician;[26] Jonathan Holland of Tussle; Devendra Banhart.

The Walter and McBean Galleries (on the 800 Chestnut Street campus) house exhibitions, workshops, and other alternative and experimental avenues for presenting work by international contemporary artists.