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After playing for a time in a Rhode Island stock company while trying to get parts on Broadway, his career got underway when he played a small part in a film, Taxi (Gregory Ratoff, 1953). A year later he began acting in short teleplays, beginning with Paso Double (for the Omnibus series). Cassavetes became typecast as a "troubled youth" in these programs and the motion pictures that were based on these plays. Among these films were Edge of the City (Martin Ritt, 1956) and Crime in the Streets (Don Siegel, 1957).

In 1956 Cassavetes began teaching method acting at a drama workshop in Manhattan. One of the group's improvisations had the makings of a film, Cassavetes thought, and he mentioned the project on Jean Shepherd's Night People radio show. While on the air, Cassavetes suggested that listeners interested in seeing an alternative to Hollywood cinema should send in money to fund his project. Shepherd's audience sent in donations totalling around $20,000; Cassavetes raised a similar amount from his show-business friends and from his own savings. With these funds he embarked (with his acting workshop and a volunteer crew) on his first film, Shadows.

Made intermittently over two years, Shadows changed the landscape of American cinema. Actors improvised within loosely defined situations and the story evolved as the shooting progressed. Everything was filmed with a hand-held 16mm camera. The score composed by jazz great Charles Mingus further added to the improvisational, cinema veritè feeling.

Unable to interest American distributors, Cassavetes screened Shadows to enthusiastic audiences in Europe (including the 1960 Venice Film Festival, where it received the Critics Award). In 1961 Shadows was released in America under the auspices of a British distributor.

Impressed by the success of Shadows, Paramount hired Cassavetes to make a series of films but released him after the financial and critical failure of Too Late Blues, his first film for them. He then directed A Child is Waiting for Stanley Kramer (and United Artists). After a falling out with Kramer, Cassavetes was given just two weeks to edit the film. Kramer re-cut the film (making it overly sentimental, according to Cassavetes). Cassavetes, infuriated, spoke out against Kramer and the film, washing his hands of the project.

Unwilling to have his vision compromised by studio heads and producers, Cassavetes acted in several films most notably Rosemary's Baby (Polanski, 1967) and The Dirty Dozen (Aldrich, 1967), for which he was nominated for an Oscar so that he could finance his own films and thereby retain artistic control.

Faces, shot and edited in 16mm over three years, was the first product of this strategy. Though not improvised on-camera as was Shadows, the film marked a return to that film's improvisational, cinema veritè style. It premiered in 1968 and was a financial and critical success, being nominated of two Academy Awards and winning five awards at the Venice Film Festival.

In the 1970s and 1980s, Cassavetes worked independently or with modest studio backing when it was offered with complete artistic control. In the latter category are Husbands (Columbia, 1970), Minnie and Moskowitz (Universal, 1971), Gloria (Columbia, 1980), and Love Streams (Cannon, 1984). Of the self-financed are The Killing of a Chinese Bookie (1976/78), Opening Night (1978), and what many consider Cassavetes' finest film, A Woman Under the Influence (1974). All feature remarkable performances by one or more actors from his regular stable of players including Peter Falk, Ben Gazzarra, and most notably, his wife (since 1954) Gena Rowlands.

Sadly, Cassavetes' final film was, as Cassavetes put it, the "aptly titled" Big Trouble (1985). Cassavetes reluctantly stepped in to direct in mid-production after Andrew Bergman, the film's writer and director, quit the project. Cassavetes considered it a disaster and was embarrassed to have his name attached to the film. Raymond Carney has persuasively argued (Film Comment: May-June 1989, p. 49) that because of the nature of the project and the final product (it hardly shows the stamp of a Cassavetes film) Love Streams rightly deserves to be considered Cassavetes' final cinematic statement.

After a three-and-a-half year illness, John Cassavetes died February 3, 1989.