Orton was originally an unsuccessful actor. He turned to writing in the late 1950s under the encouragement of his lifelong companion, K.L. Halliwell. A handful of novels the pair wrote at this time were not published, however, and it was not until 1964 that Orton had his first success, when his radio play The Ruffian on the Stair was broadcast by the BBC. From then until his death in 1967 Orton had a brilliant success as a playwright. His three full-length plays, Entertaining Mr. Sloane (1964), Loot (1965), and What the Butler Saw (produced posthumously, 1969), were outrageous and unconventional black comedies that scandalized audiences with their examination of moral corruption, violence, and sexual rapacity. Orton's writing was marked by epigrammatic wit and an incongruous polish, his characters reacting with comic propriety to the scandalous and disturbing situations in which they found themselves involved. He also wrote four one-act plays during these years, including Funeral Games (1968).

Orton's career was cut tragically short when he was beaten to death by Halliwell, a less successful writer, who immediately afterward committed suicide.