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Spoiler alert!

The plot centers on the handsome Belgian sailor Georges Querelle, who is also a thief and murderer. When his ship, the Vengeur, arrives in Brest, he visits the Feria, a bar and brothel for sailors run by the madame Lysiane, whose lover Robert is Querelle's brother. Querelle has a love/hate relationship with his brother; when they meet at La Feria, they embrace, but also punch one another slowly and repeatedly in the belly. Lysiane's husband Nono tends bar and manages La Feria's underhanded affairs with the assistance of his friend, the corrupt police captain Mario.

Querelle makes a deal to sell opium to Nono, and murders his accomplice Vic. After delivering the drugs, Querelle announces that he wants to sleep with Lysiane. He knows that this means he will have to throw dice with Nono, who, as Lysiane's husband, has the privilege of playing a game of chance with all of her prospective lovers. If Nono loses, the suitor is allowed to proceed with his affair. If the suitor loses, however, he must submit to anal sex with Nono first. "That way, I can say my wife only sleeps with assholes," Nono says. Querelle deliberately loses the game, allowing himself to be sodomized by Nono. When Nono gloats about Querelle's "loss" to Robert, who won his dice game, the brothers end up in a violent fight. Later, Querelle becomes Lysiane's lover, and also has sex with Mario.

Luckily for Querelle, a construction worker called Gil murders his coworker Theo, who had been harassing and sexually assaulting him. Gil is also considered to be the murderer of Vic. Gil hides from the police in an abandoned prison, and Roger, who is in love with Gil, establishes contact between Querelle and Gil in the hopes that Querelle can help Gil flee. Querelle falls in love with Gil, who closely resembles his brother. Gil returns his affections, but Querelle betrays Gil by tipping off the police. Querelle had cleverly arranged it so that his murder of Vic is also blamed on Gil.

In parallel there is a plot line concerning Querelle's superior, Lieutenant Seblon, who is in love with Querelle, and constantly tries to prove his manliness to him. Seblon is aware that Querelle murdered Vic, but chooses to protect him. Near the end of the film, Seblon reveals his love and concern to a drunken Querelle, and they kiss and embrace before returning to Le Vengeur.