As Ashby was entering adult life, he moved from Utah to California, where he pursued a bohemian lifestyle and ultimately became an assistant film editor through a long apprenticeship. His career gained momentum when he served as the editor of The Loved One (1965), an adaptation of the Evelyn Waugh novel that involved such New Hollywood contemporaries as screenwriter Terry Southern and cinematographer Haskell Wexler. After being nominated for the Academy Award for Film Editing in 1967 for The Russians Are Coming, the Russians Are Coming, his big break occurred one year later when he won the award for In the Heat of the Night. Ashby often stated that the practice of editing provided him with the best filmmaking background outside of traditional university study and he carried the techniques learned as an editor with him when he began directing.

At the urging of mentor Norman Jewison, Ashby directed his first film, The Landlord, an early rumination on the social dynamics of gentrification in Park Slope, Brooklyn, in 1970. While his birth date placed him within the Silent Generation, the filmmaker—who had been a habitual marijuana smoker since 1950—eagerly embraced the hippie lifestyle, adopting vegetarianism and growing his hair long before it became de rigueur.

During this period, the productions of Second-Hand Hearts and Lookin’ to Get Out —the latter a Las Vegas caper that reunited him with Voight and featured Voight’s young daughter, Angelina Jolie—were plagued by the increasingly strained relationship between Ashby and Lorimar. Filmed in 1979, Second-Hand Hearts only received a poorly-reviewed limited release in 1981 before being pulled from circulation for nearly thirty years. Belatedly released in October 1982, Lookin’ to Get Out earned a little under $1 million in returns and rentals on an estimated $17 million budget. During this period, Lorimar executives grew less tolerant of his increasingly perfectionist production (811,000 feet of film were used shooting Lookin’ to Get Out) and editing techniques; a montage in the latter film set to The Police’s “Message in a Bottle” took six months to perfect but proved to be logistically unusable due to a Lorimar agreement with the American Federation of Musicians.

Following Being There, Ashby was provisionally set to reunite with Sellers and Terry Southern on Grossing Out, a black comedy inspired by the actor’s chance meeting with an international arms dealer on an airplane. Although Southern (who had not had a screenplay go to production in a decade) was rejuvenated by the prospect of working with the duo and produced a script that was said to be on par with his 1960s oeuvre, the project went into development hell after Sellers’ sudden death from a heart attack in July 1980.

While post-production of Lookin’ to Get Out continued, Lorimar permitted Ashby to film The Rolling Stones’ 1981 American tour documentary, Let’s Spend the Night Together; the director was a longtime fan of the group. He collapsed before the final filmed concert at Sun Devil Stadium in Tempe, Arizona on December 13, 1981. Although Jeff Wexler claimed that Ashby was “partying way beyond his capabilities with the Stones,” Caleb Deschanel has said that Ashby (who directed the concert shoot on a gurney) simply had the flu. The film was well-received but gained little traction during a limited theatrical release. In September 1983, Ashby directed Solo Trans, a Neil Young concert video that was released the following year.

Longtime friend Warren Beatty advised Ashby to seek medical care after he complained of various ailments, including undiagnosed phlebitis. He was soon diagnosed with pancreatic cancer that rapidly spread to his lungs, colon, and liver. Ashby died on December 27, 1988 at his home in Malibu, California.

For the 2012 Sight & Sound Directors Top Ten poll Niki Caro, Cyrus Frisch, and Wanuri Kahiu voted for Harold and Maude, with Frisch describing the film as “an encouragement to think beyond the obvious!”

A 2018 documentary about the director was screened at the Sundance Film Festival.