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Johnny Hooker, a grifter from Depression-era Joliet, Illinois, cons $11,000 in cash from an unsuspecting victim, with the aid of his partners Luther Coleman and Joe Erie. Buoyed by the windfall, Luther announces his retirement and advises Hooker to seek out an old friend, Henry Gondorff, in Chicago, to teach him “the big con.” Unfortunately, their victim was a numbers racket courier for vicious crime boss Doyle Lonnegan. Corrupt Joliet police Lieutenant William Snyder confronts Hooker, revealing Lonnegan's involvement and demanding part of Hooker’s cut. Having already spent his cut, Hooker pays Snyder in counterfeit bills. Lonnegan's men murder Luther, and Hooker flees for his life to Chicago.
Gondorff, a once-great con-man now hiding out from the FBI, is initially reluctant to take on the dangerous Lonnegan. However, Gondorff relents and decides to resurrect an elaborate and supposedly obsolete scam known as "the wire", using a large number of con artists to create a phony off-track betting parlor.
Aboard the opulent 20th Century Limited, Gondorff, posing as boorish Chicago bookie "Shaw", buys his way into Lonnegan's private high-stakes poker game and out-cheats Lonnegan, winning $15,000 from him and making Lonnegan furious. Hooker, posing as Shaw's disgruntled employee "Kelly", is sent to collect the winnings and instead convinces Lonnegan that he wants to take over Shaw's operation. Kelly reveals that he has a partner named Les Harmon (actually fellow con man “Kid Twist”) in the Chicago Western Union office, who will allow them to win bets on horse races by past-posting.
Meanwhile, Snyder has tracked Hooker to Chicago, but his pursuit is thwarted when he is summoned by undercover FBI agents led by Agent Polk, who orders him to assist in their scheme to arrest Gondorff using Hooker. Additionally, Lonnegan has grown frustrated with his men's inability to find and kill Hooker. Unaware that “Kelly” is Hooker, he demands that "Salino," his best assassin, kill Hooker. A mysterious figure with black leather gloves is soon seen following and observing Hooker.
Kelly's connection appears effective, as Harmon provides Lonnegan with the winner of one horse race and the trifecta of another race. Lonnegan agrees to finance a $500,000 bet at Shaw's parlor to break Shaw and gain revenge. Shortly thereafter, Snyder captures Hooker and brings him before FBI Agent Polk. Polk forces Hooker to betray Gondorff by threatening to incarcerate Luther Coleman's widow.
The night prior to the sting, Hooker sleeps with Loretta, a waitress at a local restaurant. As Hooker leaves the building the next morning, he sees Loretta walking toward him. The black-gloved man appears behind Hooker and shoots Loretta dead, later revealing her to be "Loretta Salino", Lonnegan's hired killer. The black-gloved man had been hired by Gondorff to protect Hooker.
Armed with Harmon’s tip to "place it on Lucky Dan", Lonnegan makes a $500,000 bet at Shaw’s parlor on Lucky Dan to win. As the race begins, Harmon arrives and expresses shock at Lonnegan's bet, explaining that when he had said "place it" he had meant, literally, that Lucky Dan would "place" (i.e., finish second). In a panic, Lonnegan rushes the teller window and demands his money back. Just then, Agent Polk, Lt. Snyder, and half a dozen FBI officers storm the parlor. Polk confronts Gondorff, then tells Hooker he is free to go. Gondorff, reacting to the betrayal, shoots Hooker in the back; Polk then shoots Gondorff and orders Snyder to get Lonnegan away from the crime scene. With Lonnegan and Snyder safely away, Hooker and Gondorff rise amid cheers and laughter. Agent Polk is actually Hickey, a con man, running a con atop Gondorff's con to divert Snyder and provide a solid "blow off" to Gondorff's con. Hooker and Gondorff depart as the other con men strip the room of its contents.