Although he had been a cinematographer since at least 1927, he didn't shoot his first color film until 1951, An American in Paris (1951) -- which got him an Academy Award for Best Cinematography.
He became one of the most controversial cinematographers during the 1940s and 1950s in Hollywood, causing all of the MGM cinematographers to file a complaint with studio head Dore Schary and MGM exec E.J. Mannix and the AMPAS regarding his contribution to An American in Paris (1951). The charges were refuted by the film's director Vincente Minnelli and star 'Gene Kelly (I)' . Alton further incited the wrath of American cinematographers by charging that the use of light beds above the sets was not only unnatural but forced cinematographers to work more slowly. He was a brilliant iconoclast who was forced to work on low-budget features because of his flamboyant behavior, which was considered outside of the norm for a very flamboyant Hollywood.
He was replaced after two weeks of shooting Birdman of Alcatraz (1962)) by Burnett Guffey.
In 1960, following his work on Elmer Gantry (1960), he quit the movie business. He returned briefly in 1966 to direct photography for the pilot episode of the TV series "Mission: Impossible" (1966). Afterwards, he virtually disappeared. For years, even his closest friends did not know his whereabouts. In 1984, his work was honored at the Telluride Film Festival in Colorado, with a tribute entitled, "Where is John Alton?" In 1993, at the age of 92, Alton heard about Visions of Light (1992), a documentary about cinematographers that included some of his movie work. He contacted the film's producer, Todd McCarthy, and asked to attend the premiere. McCarthy, who had hoped to include an interview with Alton in the film, was astonished to hear from him. Afterwards, Alton insisted that there was nothing mysterious in his disappearance, that he and his wife had simply decided to give up the movie business and travel a bit. They had lived in France, Germany, and Argentina, and had a great time. He died in 1996 at the age of 95.
In the early 1930s, Alton traveled to Argentina to help develop that country's film industry. He helped train several cinematographers and directors, photographed over 20 films himself, and even directed several.