In 1971, James Corcoran began his career by establishing Corcoran and Corcoran in Coral Gables, Florida. This gallery showcased notable artists such as Billy Al Bengston, Jasper Johns, Roy Lichtenstein, John McLaughlin, Kenneth Price, Robert Rauschenberg, Ed Ruscha, and Cy Twombly.

Following this, Corcoran opened the James Corcoran Gallery on Santa Monica Boulevard in West Hollywood. This gallery became renowned for exhibiting works by artists like John Baldessari, Billy Al Bengston, Joe Goode, Allen Jones, Roy Lichtenstein, Ken Price, Ed Ruscha, John Tweddle, and H.C. Westermann, cementing its status as one of Los Angeles' premier art galleries over the next decade.

In 1976, Corcoran partnered with Leo Castelli and Richard Feigen to establish Castelli Feigen Corcoran in New York. This venture primarily managed the estate of Joseph Cornell, producing several important Cornell catalogues, and exhibited artists such as James Rosenquist, Ed Ruscha, and Robert Wilson.

In 1984, the James Corcoran Gallery relocated to Santa Monica, continuing to exhibit influential artists including Peter Alexander, Joseph Cornell, Dennis Hopper, David Lynch, Kim MacConnel, Bruce Nauman, Kenneth Price, Ed Ruscha, Frank Stella, and William Wegman. Corcoran also played a pivotal role in organizing major shows of West Coast assemblage art and developed extensive connections with museums and collectors in Japan, arranging notable exhibitions, including a traveling show for Ed Ruscha in Tokyo and Nagoya.

In 1993, Corcoran moved to New York and founded C and M Arts with Robert Mnuchin. Located on the Upper East Side, this gallery exhibited works by Joseph Cornell, Jackson Pollock, Mark Rothko, Ed Ruscha, and Cy Twombly, and produced numerous catalogs for these shows.

Returning to Los Angeles in 1998, Corcoran reopened the James Corcoran Gallery and coordinated private sales with his established client base. From 2011 to 2019, he was associated with Kayne Griffin Corcoran, overseeing exhibitions for artists such as Larry Bell, Robert Graham, David Lynch, John Mason, Ken Price, Jiro Takamatsu, James Turrell, and H.C.Westermann.