A red and white 1958 Plymouth Fury is built on the assembly line. The car injures one worker by slamming its hood shut on his hand; when another one sits in the driver's seat and flicks cigar ashes onto the upholstery, he is subsequently found dead. Twenty years later, nerdy teenager Arnold "Arnie" Cunningham buys the now-decrepit Fury over the objections of his friend, Dennis Guilder. At school, Arnie is bullied by Buddy Repperton and his gang, and Buddy is expelled after threatening Arnie with a switchblade. Defying his parents, Arnie begins to restore the Fury (named "Christine" by its previous owner) at a garage/junkyard owned by Will Darnell. Arnie's appearance and personality begin to change as he works; he sheds his glasses, dresses better, and develops an air of cocky arrogance. His obsession with Christine puts a strain on his relationship with his parents and his friendship with Dennis.
Dennis learns from the seller that the Fury's previous owner was also obsessed with Christine, that his daughter choked to death in the car, and that he and his wife both committed suicide in it. An attractive new student, Leigh Cabot, attends one of Dennis' football games with Arnie; Dennis sees them together and notes that Christine is now fully restored. Distracted, he suffers a severe injury that puts him in the hospital and ends his high school football career. Arnie and Leigh begin a relationship, but Leigh becomes uncomfortable sitting in Christine as the two watch a drive-in movie. The car's radio turns on by itself as Leigh begins to choke on her food, and Arnie finds the doors locked. Leigh eventually frees herself, and another patron administers the Heimlich maneuver to save her life.
Buddy and his gang vandalize Christine in retaliation for Buddy's expulsion. Arnie is so distraught that he angrily breaks up with Leigh when she tries to console him. Once he returns Christine to the garage, he is surprised to see it gradually and completely repair itself. Christine chases down one member of Buddy's gang that evening and kills him, repairing itself again afterward. Police detective Rudy Junkins questions Arnie about the death, but lets him go once Arnie provides an alibi. Later, Christine targets the rest of the gang, killing two members at a gas station and then fatally running Buddy down. The badly damaged car returns to Darnell's garage on its own; when he sits in the driver's seat, Christine kills him by pushing it forward to crush him against the steering wheel. By the time the police find the body, Christine is once more in like-new condition. Junkins again questions Arnie, who becomes angry and gives an alibi.
Leigh asks for Dennis' help to destroy Christine and save Arnie. They plan to lure Christine to the garage and smash it with a bulldozer, but Christine surprises them by emerging from a pile of scrap metal. Leigh flees while Dennis battles Christine, now being driven by Arnie; in an attempt to run Leigh down, Christine crashes into Darnell's office and Arnie is thrown through the windshield, fatally impaling himself on broken glass. Christine continues to attack, repairing itself more quickly than before, until Dennis and Leigh flatten it with the bulldozer.
The next day, Dennis, Leigh, and Junkins watch as the remains of Christine are crushed at the junkyard. Junkins congratulates the teens for stopping Christine, but they regret not being able to save Arnie. The sound of a 1950s rock and roll song spooks them, but it proves to be coming from a boombox carried by a junkyard worker. Christine's front grill twitches slightly.