Educated at Ford Street High School, John Singleton began work in advertising as a mail boy, followed five years later by a creative role at a different agency. He launched his first advertising agency SPASM in 1968. After selling SPASM in 1973, Singleton worked for some time for multinational agencies, before establishing John Singleton Advertising in 1985.
During the 1980s, John Singleton Advertising had a significant impact on Australian advertising, with a focus on a working-class, 'larrikin' tone.