21 years later, in September 1978, Arnold "Arnie" Cunningham (Keith Gordon) is an awkward and unpopular teenager, in Rockbridge, California, with only one friend, Dennis Guilder (John Stockwell). Arnie's life begins to change when he buys a used, badly battered red-and-white 1958 Plymouth Fury named "Christine" (the same car from the assembly plant), in need of extensive repairs. Due to his parents being against him keeping the car in their yard, Arnie begins to restore Christine at Darnell's Autobody, a local repair shop and junkyard, but as he spends more of his time working on the car, he discards his glasses, dresses more like a 1950s greaser, and develops an arrogant personality. Dennis investigates and learns of the car's dark past, that its obsessive previous owner and his wife both died in it and their daughter was choked to death inside the car, but Arnie does not know this. Arnie's new girlfriend, Leigh Cabot (Alexandra Paul), narrowly escapes her death when she is choking on a hamburger inside the car while on a date with Arnie.
Angry with Arnie after a shop class confrontation leads to his expulsion, lead bully Buddy Repperton (William Ostrander) and his gang, vandalize Christine. Arnie is devastated and determined to repair Christine. As he examines the ruined car, he hears the creaking of metal and notices the engine is now fully restored. Arnie tells the car, "Show me." Christine flips on its lights and restores itself to showroom quality, then, driving itself, seeks out the vandals. Moochie Welch (Malcolm Danare) is targeted first and chased down by Christine into an alley and is crushed to death. Richie and Don are caught in a gas station explosion (which sets Christine on fire); and Buddy is chased down a lonely road until he is run over and burned to death by the flaming car. Darnell (Robert Prosky), owner of the garage and junkyard where Arnie restored and keeps his Plymouth Fury, is murdered by Christine in the garage when he sits in the car and is crushed between the seat and the steering wheel. Rumors begin to spread about Arnie and the car, as state policeman Rudolph Junkins (Harry Dean Stanton) becomes suspicious of Arnie.
On New Year's Eve, Dennis and Leigh decide that the only way to stop Christine and save Arnie is to destroy the car. Dennis scratches "Darnell's Tonight"—referencing the name of the junkyard - into Christine's hood, then makes his way there with Leigh. Dennis waits in a bulldozer while Leigh heads to the office so that she can shut the door after Christine arrives, trapping the car. Christine, who has been lying in wait the entire time, shines the headlights from under a pile of trash and charges after Leigh. Christine crashes into Darnell's office in an attempt to kill Leigh, and Arnie (revealed to have been driving the car himself) is thrown through Christine's windshield. He is impaled through a shard of glass and dies, reaching out to touch Christine one last time. Dennis and Leigh engage in a fight against Christine with the bulldozer. Christine continues to attack Dennis and Leigh, repeatedly sustaining damage and regenerating. Dennis pulls Leigh into the cab of the bulldozer; the two then smash Christine, driving back and forth over the car with the bulldozer as it mocks them by playing "Rock and Roll Is Here To Stay" over the radio until at last it is too shredded to regenerate again.
Dennis, Leigh, and Junkins survive and leave behind the remains of the car. The closing shot of the film is of Christine, now having been crushed into a cube by a car crusher, as a piece of the grille slowly begins to move and "Bad to the Bone" plays.
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