London, 1967. Police discover the bodies of playwright Joe Orton and his lover Kenneth Halliwell in their flat in Islington. Orton's agent, Peggy Ramsay, looks through the flat, finds his diaries and hides them. Peggy is interviewed by John Lahr, a writer working on a biography of Orton, to whom she recounts first meeting Orton in 1964.

Peggy remembers Orton's relationship with Kenneth, which was fraught with tension and anxiety. Orton had already achieved critical and commercial success with his plays, while Kenneth was growing increasingly jealous of his partner's artistic achievements, and his own lack of involvement. Peggy gives John the diaries, which describe in detail Orton's frequent sexual encounters.

John goes to Leicester to speak with Orton's sister, who describes his early interest in acting. Despite his mother's reluctance to accept his chosen career, the young Orton (known at the time as John) leaves Leicester to begin an acting scholarship at Rada. There, Orton meets Kenneth for the first time. Kenneth is older than the other students, and is unpopular. The pair become close friends and move to a flat in Islington together. They soon become lovers. During these early years together, Kenneth teaches Orton about art and literature, and they begin collaborating on a novel. However the finished novel, is rejected by a publishing company for its risqué homosexual themes.

Orton regularly has sex with other men he meets in parks and public toilets, and sexual relations between Orton and Kenneth become increasingly infrequent. Meanwhile, Kenneth stops writing and Orton begins work on solo projects. The couple are found guilty of defacing library books and are both sentenced to six months imprisonment. In prison, Orton tells guards he is a heterosexual married man, and claims he is unaware that Kenneth has romantic feelings for him. Prison proves to be a highly creative environment for Orton, who writes a radio play that is commissioned by the BBC when he is released. With his new found success, Orton encounters Peggy, who gives him an advance for a new stage play he is working on.

Orton's new play is staged, and proves a big hit. Following a suggestion from Peggy, he changes his name to Joe. Orton convinces Kenneth, who is worried about his looks and increasing hair loss, to buy a wig. Orton then pays a stranger to pick up Kenneth and have sex with him in a public toilet. Police arrive and raid the toilets, but the duo manage to escape before they are caught.

Orton writes another hit play, called Loot, and sells the rights for a film adaptation. He is approached to write a script for a film starring The Beatles. Orton has reservations, but Paul McCartney meets with him and he decides to accept the offer. Orton wins a prestigious writing award, and takes Peggy to the ceremony instead of Kenneth. Sexual relations between Orton and Kenneth cease completely.

Orton and Kenneth go on holiday together to Morocco, where they have regular sex with young locals. Brian Epstein contacts Orton to express his concerns about the references to drugs and homosexuality in his film script. Kenneth is angered when Orton continues to work during their holiday, and the pair consider separating.

On returning home, Orton receives word that his mother had died. He is unaffected by the news but goes back to Leicester for the funeral. In London, Kenneth's neuroses worsen, and he arranges to see a psychiatrist. Orton again asks Kenneth about ending the relationship. Having grown increasingly jealous and disillusioned with Orton, Kenneth bludgeons him to death while he sleeps, before killing himself. The police discover their bodies. Orton and Kenneth have separate funerals, but later their ashes are combined and scattered.