The movie stars Keith Gordon as Arnie Cunningham, a typical mild mannered high school nerd with only one friend, a childhood companion named Dennis Guilder (John Stockwell), a popular jock. Arnie's life begins to change when he discovers Christine, a red 1958 Plymouth Fury in serious need of repair. Arnie begins to restore Christine to her original beauty, but as he spends more and more of his time repairing her, those in his life notice that he is changing as well. Formerly shy, Arnie develops a cocky arrogance. Dennis, as well as Arnie's new girlfriend Leigh Cabot (Alexandra Paul) discover that the car has a deadly past. The previous owner, Roland LeBay, became consumed with Christine and he paid for it with his life. Leigh and Dennis try to save Arnie from a similar fate. They realize that the only way to save Arnie is by destroying Christine. Christine, however, isn't ready to give up Arnie without a fight.
During the film a group of bullies from school form together and tear the car apart with sledge hammers, pry bars and knives etc. The gang bears a grudge against Arnie after a shop class confrontation prior to Christine that results in the gang's leader, Buddy Repperton (William Ostrander), getting expelled for threatening Arnie with a switchblade.
The prolonged gang attack on Christine leaves her totally ruined, fit only for the smelter. Arnie sees the wreck of Christine the next day and is totally shocked that all the work he put into restoring the car has been destroyed. Arnie then shows his slow descent into darkness, evidenced by angrily blaming Leigh for the wreck, and displaying further problems with his temper, getting into arguments with his parents and having a scuffle with his father, which Arnie wins by grabbing his father by the neck. He is determined to restore Christine yet again to her former glory. The next day he goes back to the garage where Christine is.
As he looks her over, he turns his back and hears the crinkling of metal behind him. Arnie looks at Christine again and sees that part of her engine is now repaired. Arnie simply smiles and says, "Okay... show me." Christine, flickering her headlights on, then comes to life and restores herself so she looks good as new. Subsequently, Christine seeks out and kills the individual members of the gang who destroyed her, one by one.
In one incident, Christine has a long chase with one of the boys, during which Christine could easily kill the boy, but maliciously toys with the boy simply to terrorize him further. In the end, Christine tires of her game and crushes the boy to death against the wall of a building, which bisected him in the process (as reported by the police). In another incident, she destroys a gas station (trapping and burning two of the vandals inside) before running down and burning Buddy Repperton as he flees the scene in terror. She also kills Will Darnell (Robert Prosky), the grouchy, foul-mouthed owner of the garage where she resides, by crushing him in the front seat. In each of these night-time attacks Christine is badly damaged (crushed or totally burned, etc.) but miraculously regenerates herself every time so she looks good as new, like she just drove off the production line in 1957.
Dennis and Leigh both notice Arnie's changes. They talk about it at the Guilder's house on New Year's Eve, where they reason the only way to stop Christine and save Arnie is to destroy the car. Dennis then says that he is going to Arnie's for the New Year, and Leigh urges him to be careful. After she leaves, Arnie pulls up to the Guilder's house in Christine, picks up Dennis, and drives off. During the ride to the Cunningham's, Arnie does a variety of things: drinks beer, takes his hands off the wheel, and tells Dennis about how strong the bond between he and Christine is. The next day, Dennis scratches "Darnell's Tonight" into Christine's hood, and drives off with Leigh. They go to Darnell's and wait in a bulldozer. Dennis then tells Leigh to wait in the office so she can shut the door after Christine arrives. This way the car will be trapped. When Leigh exits the bulldozer and heads for the office, Christine's headlights shoot out of a pile of garbage, and the car charges at Leigh. Arnie pays the ultimate price when he dies after he crashes Christine into Darnell's office in an attempt to kill Leigh. Arnie is thrown through Christine's windshield and is impaled on a shard of glass, killing him. Christine continues to attack Dennis and Leigh, sustains damage, and regenerates even after Arnie is killed. After Dennis and Leigh destroy Christine, the car is compacted into a cube and tossed into a junkyard. As the camera zooms in on the crushed cube that was formerly Christine, a piece of the grill slowly bends back into shape.