On the outskirts of Santa Ynez, two young people named Jimmy (Joshua Davis) and Suzie (Melody Thomas Scott) are riding bicycles along the highway. A vehicle comes from behind and drives right up on them, trapping them on a bridge. The sinister black sedan toys with them before killing them, crashing Suzie against the concrete barrier and then sending Jimmy plummeting to his death off the bridge. The car gives an otherworldly roar from its engine, and an ominous staccato blaring of its horn.
Shortly after, near the entrance to Santa Ynez, a young hitchhiker named John Morris (John Rubinstein) observes a local named Amos Clements (R.G. Armstrong) chasing his wife, Bertha (Doris Dowling), out of their house and striking her. The young man attempts to intervene, but Amos demands he leave. As Amos and his wife go back in the house, the young man spies a black car coming up the road, preceded by a high wind. The driver almost hits the young man, and he screams obscenities after it. Suddenly, the car brakes to a halt, and backs up, running over the young man several times before driving off. Amos sees this from a window in his house, and calls the police.
Meanwhile, police officer Wade Parent (James Brolin) is waking up with his girlfriend Lauren (Kathleen Lloyd), a local schoolteacher. Wade is a widowed father of two young girls, Lynn Marie (Kim Richards) and Debbie (Kyle Richards). Lauren wants Wade to socialize her with the girls so they can be up front about their relationship, as she is currently sneaking out of the house after she sleeps there, but the girls are already listening to the entire conversation just outside the bedroom door.
After Wade drops the girls off at school on his motorcycle, he is summoned to the Clements house in the aftermath of the hitchhiker's death. Several other officers, including Sheriff Everett (John Marley) are interrogating Amos about the incident. Amos provides scant details about the car, and several of the officers note that Amos' wife seems to be rather quiet. Everett (John Marley) is furious that someone in his town has been murdered, despite the fact that Morris was not a local. At first, their vague description of the car turns up a report that someone spotted it driving out of town into a nearby locality, but when Suzie's body turns up, it's clear that something larger is going on. Police officer Luke (Ronny Cox) is terribly upset about it; Jimmy's body has not yet been discovered, and there is suspicion about his involvement in Suzie's death. Luke and Jimmy are close, and Jimmy has lied to Luke about his whereabouts, apparently in an attempt to conceal his relationship with Suzie. Luke is a recovering alcoholic; his wife Margie (Elizabeth Thompson) tells Wade and Lauren that Luke has been sober for two years.
Later on that evening, Amos and his family are taken into the office for questioning after someone reports him abusing his wife again. Everett pleads with Bertha to file an official report about her husband's abuse so Everett can arrest him, but Bertha refuses. Everett and Bertha have history together, and Everett tells Wade that Bertha was his first love when they were both young. He watches sadly as she and her son get into their truck and drive off, while Amos goes across the street to a bar. Everett invites Wade to have a drink with him at the tavern, and Wade tells him he'll be along shortly. But as Everett crosses the street, he sees Amos crossing as well, and suddenly the black car roars to life down the street, heading right for Amos. Amos dives for the curb, and the car instead ends up running over Everett. Wade questions the few citizens who witnessed the incident, including an old Navajo woman who doesn't speak English. Chas (Henry O'Brien) is another Native American officer who translates for her as she describes what happened, but he refuses to translate one thing she says, telling Wade it's "Indian talk...she's a crazy old woman." But the dispatcher, Donna (Geraldine Keams), is also Navajo, and she later tells Wade what Chas would not: the woman claims there was no driver in the car.
Wade assumes the Sheriff's duties, and requests that roadblocks be put up. He also tells Luke to contact the school and cancel parade rehearsals for the next day. However, a distraction occurs when Jimmy's body is discovered by a fisherman. Luke is despondent over the deaths of both Everett and now Jimmy, and he begins to secretly drink alcohol again.
The parade rehearsal happens as scheduled, with Lauren and Margie leading the children. A high wind whips up soon after, and the car appears, shadowing the parade behind a line of tents. Suddenly it bursts through onto the main roadway, spooking the horses and causing them to stampede and throw their riders. The car rushes after the panicked group, striking several adults, including a police officer who was watching over the parade rehearsal. Lauren and the other adults lead them into nearby cliffs to avoid the car, and the large group dashes into a small fenced-in cemetery nearby. Amazingly, the car refuses to enter, despite the fact that it could easily pass through the gate. Lauren distracts the car by taunting it, while Margie sneaks out of the cemetery. The car almost runs her down as she runs across the roadway, but she makes it and summons help using the police officer's radio. The car returns to the cemetery entrance and Lauren continues to curse it, calling the driver a "chicken shit" and hurling a tree branch at it, striking the hood. The car seems furious, whirling in circles and striking one of the entrance pillars to the cemetery, but still it will not enter. Finally, the group hears the approach of police sirens, and the car speeds off. One frightened woman finally finds her voice and screams after the car, "Cat poo!", and the ordeal is finally over.
The car speeds off and is spotted by one officer, who follows it up onto a cliff, but it surprises him and turns the tables, slowly pushing him to his death over the cliffside. As Wade rushes to the scene, the car emerges from the hillside and confronts two police cars driving side by side in a blockade. They hope to force the car off the road, but instead it goes into a barrel roll straight for them, rolling over their cars and causing them to crash. The officers inside are all dead, but the car emerges unharmed. Wade then arrives and confronts the car when it ominously rolls to a stop. He fires on it from close range, but the bullets do no harm, not even to the tires. Wade then walks up to the car. As he does so, the door suddenly flies open, knocking him down into a ditch. Wade then wakes up in the hospital, dazed from the experience. He talks with the remaining deputies about keeping the roadblocks up, and Lauren says she will stay at Wade's house with the girls. Wade sends Chas with Lauren to her house to get her things, and then he confronts Luke about why he did not cancel the parade rehearsal as instructed. Luke admits he's been drinking again, unable to cope with the grief of losing both Everett and Jimmy in the same day, not to mention all the other officers who are also now dead after their confrontations with the car.
Chas escorts Lauren home, but she notices he is concerned about his family. She tells him to check on his family while she packs an overnight bag, and he leaves. As he drives back up the road, the car rolls silently out of the darkness and waits for him to pass, suddenly roaring to life and taking off in the opposite direction for Lauren's house. A strong wind whips up, and Lauren rushes inside, terrified. She calls Wade in a panic, terrified as she hears the engine of the car approaching. Behind her, the headlights can be seen in her window, and as she talks to Wade on the phone, suddenly the headlights levitate off the ground and the car bursts through her house at high speed, killing her in the process, before driving out the other side and off into the night.
Wade and his deputies soon after investigate the remains of the house. Luke understands the significance of what has happened. He comments that the car couldn't enter the cemetery because it was hallowed ground, and it had a vendetta for Lauren because she cursed it. Wade is skeptical, but even he can't explain why the car was able to levitate through Lauren's house.
Heartbroken over Lauren's brutal death, Wade is determined to avenge her. He enlists Amos, who works with dynamite, to set up a trap for the car; they will lure it into a quarry and explode the quarry wall, burying it. Wade goes home to check on his children, who are being tended to by Margie. Finding all of them asleep, Wade leaves a note behind telling Margie to take care of the kids. Passing through his garage, he is startled to find the car parked inside there, waiting for him. It traps him in the garage, threatening to run him down each time he makes a move for the door. Margie awakens, unaware of what has transpired and still expecting Lauren to arrive any minute. Wade warns her the car is there and she runs back into the house. The car begins to rev its engine to an ear-shattering decibel, causing the glass in the house to shatter. Margie and the children are terrified, until Wade manages to escape the garage and get to his bike. He takes off with the car chasing him, leading it away from the house and off to the quarry where the trap awaits. The men aren't finished setting up the charges, though, and Wade has to keep the car distracted by circling with it inside the quarry. Finally he overturns his bike and makes a leap for the rope the men have lowered down to him from the cliff; the car realizes what is happening and makes for the road, roaring up the cliffside toward Wade and the others. Wade and Luke stay right at the cliff's edge, luring the car closer, until finally they leap to the side and the car goes flying off the cliff into the quarry below. The men ignite the dynamite and the entire cliffside explodes, burying the car under tons of rubble. In the resulting fireball, a huge demonic apparition forms, vanishing as the fire subsides and the smoke clears. Wade and the others are sure they've buried the car for good.
The film concludes with scenes of the car driving around Los Angeles, presumably waiting to claim new victims.