Aging Irishman Leo (Albert Finney) runs an unnamed eastern city during Prohibition. Leo's chief adviser - and the only man he trusts - is the intelligent, nonviolent Tommy (Gabriel Byrne). Leo controls the mayor and the chief of police. However, the Italian Johnny Caspar (Jon Polito) - whose chief henchman is the brutal, bisexual Eddie Dane (J.E. Freeman) - is becoming a threat to Leo's supremacy. Caspar tells Leo that he wants the unlikeable "Bernie" Bernbaum killed, because Bernie has been cutting into Caspar's gambling profits by selling information about fixed fights to bettors. But Leo refuses to allow this because Bernie is the brother of Leo's tough mistress Verna (Marcia Gay Harden). Tommy tells Leo to allow Bernie's murder, because Verna isn't worth their going to war with Caspar. Tommy, fearing Leo's life is in danger, confesses to him that he also has been sleeping with Verna. Leo beats Tommy up and kicks him out of his organization. Caspar becomes the major power in town, taking control of the mayor and chief of police. Much to Dane's chagrin, Caspar recruits Tommy into their operation. Tommy must prove his loyalty by killing Bernie in the wilderness, at Miller's Crossing (hence the title of the movie). He allows the pleading Bernie to live, on the condition that no one finds out Bernie's still alive. Dane doesn't believe Tommy killed Bernie, so he takes him back to Miller's Crossing with the intention of finding Bernie's body. A body is there, with its face shot in. Bernie has murdered Dane's male lover, Mink - but Dane can't recognize the corpse. Bernie blackmails Tommy by saying he'll come out into the open unless Tommy helps him kill Caspar. Tommy convinces Caspar that Dane and Mink - whom Caspar thinks is still alive - are secretly selling information about Caspar's fixed fights. Before Dane can kill Tommy, Caspar brutally kills Dane. Tommy maneuvers Caspar to rendezvous with Mink; instead Caspar finds Bernie, who kills him. Tommy tells Bernie that they'll blame the murder on Dane, whom Bernie thinks is still alive. Tommy takes Bernie's gun, supposedly to hide the evidence. But then Tommy reveals that Dane is dead and, in revenge for being blackmailed, points Bernie's own gun at him. Bernie again pleads for his life, thinking Tommy hasn't got what it takes to kill anyone. Tommy blasts him between the eyes. Leo marries Verna and invites Tommy to work for him again, but Tommy turns him down.