He started writing films for Roger Corman, including The Tomb of Ligeia in 1964, and was later part of the New Hollywood wave of filmmaking.

He collaborated with Tom Cruise on the films Days of Thunder (1990), The Firm (1993) and the first two installments of the Mission: Impossible franchise (1996, 2000).

He took an acting class with Roger Corman taught by Jeff Corey where his classmates also included Jack Nicholson (with whom he shared an apartment), Irvin Kershner, and Sally Kellerman.

Towne started writing for television on such programs as The Lloyd Bridges Show, Breaking Point, The Outer Limits, and The Man from U.N.C.L.E..

Towne later claimed his main contributions were removing the ménage à trois relationship between Bonnie, Clyde, and W.D., making some structural changes.

The film was a huge success and although Towne's contribution was credited only as a "special consultant", he began to earn a reputation in Hollywood as a top script doctor.

Towne received acclaim and was nominated in the Best Original and Adapted Screenplay categories for his scripts The Last Detail (1973), Chinatown (1974), and Shampoo (1975).

[16][17][18] He later said it was inspired by a chapter in Carey McWilliams's Southern California Country: An Island on the Land (1946) and a West magazine article on Raymond Chandler's Los Angeles.

[21] Towne did uncredited work on Deal of the Century (1983), 8 Million Ways to Die (1986) ([22]), Tough Guys Don't Dance (1987) and Frantic (1988).

[citation needed] He told writer Alex Simon, "In the interest of maintaining my friendships with Jack Nicholson and Robert Evans, I’d rather not go into it, but let’s just say The Two Jakes wasn’t a pleasant experience for any of us.

"[23] In a November 5, 2007, interview with MTV, Jack Nicholson claimed that Towne had written the part of Gittes specifically for him and had conceived Chinatown as a trilogy, with the third film set in 1968 and dealing in some way with Howard Hughes.

A project Towne had long sought to bring to the screen came to fruition in 2006 with Ask the Dust, a romantic period piece set in Los Angeles based on the novel by John Fante and starring Colin Farrell and Salma Hayek.

He told The New York Times "I think melodrama is always a splendid occasion to entertain an audience and say things you want to say without rubbing their noses in it.

Morris describes him as an “elliptical figure” whose career exemplifies a certain characteristic mode of working in the film industry, marked by collaboration, shared or changing roles.

[27] Morris's 19,744-square-foot (1,834.3 m2) painting installation in the entryway to the Lever House in Manhattan, commissioned by the Public Art Fund, was also titled "Robert Towne".

[32] According to Sam Wasson's The Big Goodbye: Chinatown and the Last Years of Hollywood, Towne was addicted to cocaine during this period and was occasionally violent, which led to a bitter divorce and custody battle over their daughter Katharine (born 1978).