Trish Jenner and her brother Darry are traveling home from college for spring break. As they drive through the Florida countryside, an old truck threateningly tailgates them but eventually passes. They later observe the same truck parked next to an abandoned church with the driver sliding what appears to be bodies wrapped in blood-stained sheets into a large pipe sticking out of the ground. Having noticed their car pass by, the driver pursues and runs them off the road.
After the truck drives off, Darry convinces Trish to go back to the church. Upon investigation, Darry hears noises coming from within the pipe and crawls inside with Trish holding on to his feet, but ends up falling in. At the bottom, he finds a dying man with stitches running down his stomach, hundreds of other bodies sewn to the basement's walls and ceiling, and the bodies of Kenny and Darla, a prom couple that had gone missing twenty-three years prior. After escaping, the two flee the scene and attempt to contact the police at a diner, where they are phoned by a strange woman who tells them they are in danger. She plays the song "Jeepers Creepers" on a record player, and confused, they ignore her warning and leave with two police officers providing a security escort. As they travel, the police learn that the church has caught fire and any potential evidence has been destroyed. The police are then attacked and killed by the driver, who loads their bodies into the truck. Witnessing the aftermath, Trish and Darry drive off in terror.
The pair stop at the house of an elderly and reclusive woman, begging her to call the police. The woman complies until she notices the driver hiding in her yard, who kills her before revealing its inhuman face to Trish and Darry. Trish repeatedly runs the driver over with her car but is left horrified as she sees a giant wing tear through its trench coat and flap in the air. The pair leave and drive to a local police station, where they are approached by psychic Jezelle Gay Hartman, the woman who called them at the diner. She tells them the true nature of their pursuer: It is an ancient creature, known as "the Creeper," which awakens every 23rd spring for twenty-three days to feast on human body parts, which then form parts of its own body. She also tells them that it seeks out its victims through fear, and by smelling the fear from Trish and Darry, it has found something it likes.
The wounded Creeper arrives at the police station, cuts off the power, and eats several prisoners to heal. The Creeper is swarmed by police but kills a number of them and evades capture. Trapped, Jezelle warns Trish and Darry that one of them will die a horrible death. Darry demands to know who, and Jezelle looks at Trish. The Creeper finds them but spares Jezelle before cornering Trish and Darry in an upstairs interrogation room. After sniffing and tasting them, the Creeper throws Trish aside and chooses Darry. Trish offers her life for her brother's, but the Creeper escapes out of a window and flies away with Darry. The next day, Trish is picked up by her parents, and Jezelle returns home in regret. In an abandoned factory, it is revealed that the Creeper has removed the back of Darry's head and taken his eyes.
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