In 1957, Conner and his wife moved to San Francisco, where he became part of a small, tight-knit artist community that included poet Michael McClure, whom he had known since grade school, Joan and Bill Brown, Jay DeFeo, George Herms and Wallace Berman. Unlike New York, there was no established market and galleries were fluid sites that were largely community nexus points for arists, rather than venues to sell work to collectors. During this time, Conner had already begun to work in his diverse and prolific manner, creating assemblages, paintings, collages and his first film, A Movie in 1958, with found footage before he even owned a camera.

Throughout the next decade, as pop art and social unrest dominated people’s attention, Conner was quietly creating an extensive, obsessive and singular body of work, driven by, among many other things, a perpetual fear of being “pinned down” by a recognizable style. While he resolutely operated outside of the mainstream, even “retiring” from the art world for a time in the late 1960s and early 1970s, much of Conner’s work is responsive to the countercultural currents of the era. His assemblages of the late 1950s and early 1960s speak to postwar anxieties, the shock of the atom bomb, the tension of private and public expressions of sexuality and rising consumer culture. Films like Vivian and Cosmic Ray are quick-cut found footage assemblages that tell of the advent of music videos and short attention spans and deconstruct the formal qualities of film. Intricate all-over drawings from the 1970s are meditative, obsessive, influenced equally by the rise of hippie and drug culture and the popularization of eastern philosophies in the west. His collages made from eighteenth century engravings are dense, lyrical and surreal. He photographed the San Francisco punk scene of the 1970s, made celestial photograms of angels, inkblot drawings that speak through symbols and pulled off a good deal of conceptual pranks and fits. Conner’s body of work is stunning in its range, its unwavering commitment to artistic integrity and unending search for new challenges and mysteries. He has been described as a "cosmological artist," creating “indecipherable missives from a self-contained universe.” (Hatch, Looking for Bruce Conner)

Conner’s work was the subject of major retrospectives at Walker Art Center, 2000 BC: The Bruce Conner Story Part II in 1999 and, after his death in 2008, at The Museum of Modern Art, New York, Bruce Conner: It’s All True in 2016.