In the mid-1970s, Salvador Dalí offered Caitlin the opportunity to model for him, but Gala, his wife, was not in favor of the project so it was canceled.

She relocated to Seattle to appear as Celia in As You Like It, Gwendolyn in Travesties, and Eylie in Ladyhouse Blues at ACT/Seattle, then returned to New York to play the double roles of Belle and Mrs. Cratchit in A Christmas Carol at Playwrights Horizon. When A Christmas Carol closed, O'Heaney moved to Los Angeles, and five weeks later she was cast as Anna Marie Hollyhock in the 1978 ABC comedy series Apple Pie, which was produced by Norman Lear, directed by Peter Bonerz, and starred Rue McClanahan, Dabney Coleman, Jack Gilford, Derrel Maury, Mike Binder and Richard Libertini. This was a highlight of O'Heaney's career. She says with regard to the experience, "It was pure magic and incredible fun working every day with these wonderful people!"

O'Heaney appeared in the television movie The Seeding of Sarah Burns in 1979 and as waitress Lurleen Hamett in ABC's One Life to Live. She played the female lead, Amy, in the horror feature He Knows You're Alone (1980), which was Tom Hanks' first feature film. In 1982, she was cast in the lead female role of Sarah Stickney White in ABC's Tales of the Gold Monkey, also starring Stephen Collins, Roddy McDowall and Jeff MacKay. She also appeared as 1930s Hollywood Actress Dolores Farrar in Woody Allen's 1982 film Zelig, and Allen would cast her again in The Purple Rose of Cairo in 1985. She played Miss Farmer in the 1987 film Three O'Clock High.

Although she was active in television throughout the period, O'Heaney did not appear in any feature films for nearly two decades, then returned in 2002 as Mrs. Woodbridge in The Emperor's Club with Kevin Kline, O'Heaney's colleague and friend at Juilliard. She also played Aunt Fran in the 2005 film Brooklyn Lobster, and most recently appeared in the 2007 independent feature Asylum Seekers. O'Heaney wrapped the feature film Late Phases, a thriller directed by Adrian Garcia Bogliano, in June 2013 in which she played the role of Emma.

In 2006-2007, O'Heaney performed on radio with Air Pirates Radio Theater.

In February 2008, she wrote the music and lyrics for an anti-war Environmentalist song titled "Who Have We Freed?" which she recorded with Pete Seeger. She and Seeger have performed "Who Have We Freed?" at various environmental/anti-war festivals in and around New York.