We open on a long country road, where Trish (Gina Phillips) and Darry (Justin Long) are driving back home during Spring Break. As the two are driving down the road we learn that they are taking the long way home. Darry claims that the reason they are doing this is because Trish is trying to avoid getting home quick in order to postpone talking about her boyfriend from college. It is implied that Trish and her boyfriend are no longer together. As they are driving they see an RV up ahead of them. Both try to figure out what the vanity plates message is a game the two like to play.
As they pass the RV and begin driving further down the road, we see that behind them that the RV turns off the road quite suddenly. Then we see a beaten up van coming down the road behind Trish and Darry, unbeknownst to them. The van approaches them quite quickly and tail gates them, honking the horn insistently. Trish yells at Darry to let him pass and Darry keeps swerving on the road. Finally, Darry moves over to the oncoming traffic lane and lets the van pass. As the van passes, we see the license plates says, BEATNGU.
Trish mentions that the encounter with the truck reminded her of Kenny and Darla. It was said that Kenny and Darla were drunk driving and that their bodies were never recovered only the vehicle was found. Darry disagrees and says that they just werent able to find her, Darlas, head or Kenny. Darry chalks it up to a generational cautionary tale of drinking and driving. Despite this, Trish is still spooked and claims that she had always heard it was true that Kenny and Darla attended Wheaton Valley High and were part of the class of 78. Trish then tells Darry that when she first heard the story she thought she would die on that highway. The two then start bickering over whether or not Darry will get the point for the vanity plate on the van, claiming it read as beating you, since he didnt call it right when he saw the plate.
The two stop on the side of the road to urinate, Trish asks her brother if he had talked to their mother. He claims that he only told her that he would be home for break. Trish asks how her mother sounded, particularly if she sounded weird. As Trish gets back in the car she notices that Darry has a bag full of laundry for their mother to do. Trish then claims that something is wrong with their mother, which Darry denies. Trish says that he is unable to notice anything beyond his own existence and insists that their mother isnt happy. At that point, Darry notices the beaten up van that tailgated them from before. It is by an old run-down church. As they slowly pass the van, we see that the driver is a guy with his face covered, wearing a hat and a dark trench coat. Both notice that he is dumping something wrapped in a bloody sheet down a pipe. On the drivers second trip to the pipe he notices the two watching him.
The two begin asking each other what he was doing with the bloody sheets wrapped with rope. Trish tells Darry to get them out of there, while Darry tells her to grab his cell phone in his gym bag. She finds the cell phone and notices that the van is now pulling out from the church and begins to follow them. Trish tries to use the phone but sees that his battery is low and despite the fact that Darry has a power plug for it, her lighter doesnt work. The van is now catching up to their car at unnatural speed. As he catches up to them he smashes into the back of their car several times, finally running them off the road and into a field. The van continues on down the road.
After Darry fixes the trunk of Trishs car, he stops and says that they need to go back. They both know that it was a person in the sheet and Darry wants to go back and check that the person isnt still alive. Trish doesnt want to and would rather get to a phone and call the cops. Darry argues that they are too far away from a phone to be able to save the person if they are still alive. He finally convinces her by asking if it were her back there.
They head back to the church, which is surrounded by crows. Upon approaching the pipe, which smells terrible, Darry claims to have heard something down there and he shines a light down there. So he climbs into the pipe, asking Trish to hold onto his feet. As he is shining the light down in the pipe he claims to see something, which happens to be rats. Trish and Darry start screaming and in the commotion Trish lets go of Darry, leading Darry to fall down the pipe. While Darry is down there he notices the bloody sheet that the creepy guy threw down the pipe. He kicks it to see if the person is alive, and when it doesnt move he turns to yell up to Trish, when all of a sudden the person in the sheet grabs his leg. The person in the sheet starts to thrash around and Darry uncovers his face to find it is a boy not much older than him. His face is blue and he starts pointing to his stomach. When Darry rips open the sheet he sees that the boys stomach has been opened up and sewn back together. The boy in the sheets starts to mumble something inaudibly and when Darry leans in to hear him better, the boy dies. Darry then goes back to the opening of the pipe and tells Trish that she needs to go back to the road and get help by flagging someone down. Darry claims that he is going to find a way out. Before Trish can leave he tells her that if she sees the old van that she needs to run back to the pipe and let him know.
Darry then heads further into the basement and sees more bodies wrapped in sheets. He then sees that there is an opening into a room. As he inspects the room he finds a bunch of weird instruments and bottles. As he is looking he notices that his show is untied and upon bending down to tie it his flashlight shines on the wall behind him showing a collection of naked human bodies, all arranged weirdly onto the wall. All of a sudden, something drips onto Darrys shoe. He shines his flashlight up to the ceiling and sees hundreds of bodies all over the walls. Trish is out on the road watching for cars, which there seem to be none approaching from either direction. While she is out there we cut back to Darry down in the basement where he has found an opening leading out of the basement. As he approaches it he notices two bodies sewn together in the corner. The womans sewn on head is placed on the guys shoulders, their arms sewn together leading to their hands intertwined with one anothers. Darry notices a class ring on the guys finger which says Wheaton Valley High.
Back on the road, Trish is facing oncoming traffic in the left lane. While she is facing this way, behind her we see headlights approaching in the distance. Finally, Trish looks behind her and sees what looks to be a beaten up van coming towards her. She hops into her car and tries to start the car, but it seems as though the cars clutch is stuck in gear. As the vehicle comes closer we see that it wasnt the beaten up van but a beaten up truck with hay in the back. As she relaxes from having scared herself thinking it was the creepy guy, her brother, Darry pops up by her window looking completely in shock.
The two begin heading down the road again, Trish trying to get Darry to say something. Trish notices that they are low on gas and claims that they need to stop as she passes a sign that reads they are entering Pertwilla. At that point, Darry speaks up mentioning that the tales about Kenny and Darla were true and that she did lose her head.
Trish pulls into a diner with a gas pump. As they get out of the car they are discussing that they need to call the cops and Darry needs to tell them what he found. At that point, we see the beaten up van pass by the diner, heading back to the run-down church. Both run into the diner, asking for a phone to call the cops. Everyone in the diner looks at them puzzled. Finally, the waitress goes to call the cops. Trish turns to her brother, trying to snap him out of his frightened state when the payphone in the diner rings. Trish picks it up and a woman asks if they have seen the cats yet. The woman on the phone explains that she had seen her and Darry with lots of cats. Trish, confused, asks how she knows Darry. At this point, Darry takes the phone and starts asking the woman who she is. The woman continues on proving that she knows who they are by describing Darrys torn shirt, bloody hand, and rose tattoo on his stomach. She tells them that they have found its house of pain. She explains it to be a hungry thing that will not stop coming after them or anyone else it wants. She proclaims that once it has the scent of something it likes, it cant stop. She says that she saw the awful truck/van, too, with the weird license plate. Darry asks, Beating you? She tells him no, and to think about it. Then she tells him to listen to something. On her speaker she has playing Jeepers Creepers (Jeepers Creepers, whered you get those peepers/Jeepers Creepers, whered you get those eyes. She tells Darry that when he hears that song to run because it means something terrible for him. Darry ends up hanging up on her.
It is now night, and Darry has already relayed what he saw to two cops, a Black woman and a white guy. Darry begins questioning Trish if she believes him. The gentleman cop comes over and lets them know that there is a unit on its way over to the church. But the cop questions what Darry saw, claiming that Kenny and Darla would have been bones by now since the crash happened over 20 years ago. Darry insists he knows what he saw retelling that there were at least 600 bodies all stitched together like a quilt. Then the waitress comes over asking if his car is over by the pumps. They run outside and see that their clothes are all over the floor. The waitress says that they saw some guy standing over by their car, sniffing their clothes. The people in the diner say that they saw him head back down the road towards the church again. Darry claims that the creepy guy knows what we saw and that he is after them now. As he is picking up his clothes, he notices that there is a handprint on the door handle the handprint is quite ashy. As Trish looks at the print, she notices a shadow in the sky and the sound of wings up above them. But when she looks up she sees nothing.
Darry and Trish are back on the road, this time with the two cops driving behind them, escorting them. Both question how he was able to get back to the church and diner so quickly and why he was sniffing their clothes. The cops then get a call from central letting them know that the church is now burning out of control. Back in Trishs car, Trish turns on the radio and begins surfing through the channels. She passes a modern pop song of Jeepers Creepers. Darry turns back to it saying it's the song the woman was talking about on the phone. Trish and Darry begin bickering. Back in the police cruiser, they get back the results from the dust on the car handle which is dead skin. Suddenly, the cops hear a thud on their hood of their car. Back in Trishs car, still bickering over the song, we see that the creepy guy is on the hood of the police car. The woman cop looks out and is thrown out of the car, while the male cop driving gets his head chopped off, which is then thrown onto the windshield of Trishs car causing them to swerve to a stop. They get out of the car and Trish begins walking to the police car, seeing someone moving in the car, but then on the road sees the severed head of the cop. Trish runs back to the car and they look out and watch the creepy guy get out of the car, whistling the Jeepers Creepers song. Both watch as he eats the cops tongue. They leave, despite Trishs car giving her some issues. We then see the Creeper (Jonathan Breck) throw the cops body into the back of his van.
Trish stops the car after Darry insists she slows down. To their left is a house, which Trish takes as an opportunity to get help. As they walk towards the house, Trish notices that the owners of the house have a scarecrow in their garden. The two are greeted by an old woman Trish asks to use her phone, but the woman explains that she does not have one. She asks what Trish needs with a phone anyway and Trish tells her that she needs to contact the police. The woman says that she doesnt want the police out near her house because they are trying to get her to get rid of some of her cats. Once Trish mentions that someone has been killed she turns on the light, concerned that it was one of her cats. We then see that there are at least 20 cats in her home. Darry tries to get Trish to leave when the lights on the womans porch go out. All of a sudden all the cats in the womans house go towards the screen and begin growling. The woman asks if they brought anyone else with them, looking off to the right. When Trish and Darry turn around they see the Creeper where the scarecrow was. The old woman comes out from the porch with a shotgun and tells him to get out of her yard. When the Creeper moves from the scarecrow the old woman shoots, but instead of hitting him she hits the scarecrow. The Creeper then jumps from the ground and scurries across the old womans roof, breaking into her house. The woman goes into her house despite the pleas from Trish and Darry. From outside, they hear two gun shots. Then they see the old woman by the inside door of her porch. They see that the Creeper has killed her and was propping her up. Trish and Darry finally see the face of the Creeper (he looks like a monster with bat-like features and his eyes are all clouded over as if he is blind).
Trish and Darry run to their car and the Creeper follows, jumping onto their hood. Trish reverses the car and tries to run over the Creeper to no avail. She then waits until he is close enough and hits him with her car. She then reverses and runs over him a couple more times. Darry stops her and they watch as the Creepers wings come out. The Creeper attempts to fly away but is too damaged. Trish runs over him one more time and they head off to the Poho County Police Station.
In the police station we see that a guy has been picked up for trying to steal a car. Trish is on the phone with her mother, who is upset along with Trishs dad. Trishs mom tries to go get them, but Trish explains that they dont want to wait for her. They are just going to drive home themselves. Darry notices a board of missing people, one missing person being a child. Just then a woman comes into the police station saying Trishs name. We find out that her name is Jez (Patricia Belcher). She tells them about how she had seen them with the bodies in the cellar and then seeing them with a bunch of cats. Darry figures out that this is the woman on the phone from the diner. Jez explains that she has dreams and that she has seen them two. Jez goes on to tell them about the Creepers ritual. Every 23rd of Spring, the Creeper is allowed to eat for 23 days. While Jez is explaining this, we notice that the beaten up van pulls up to the police station and the injured Creeper hops out and makes it way to the back of the police station. He eats things that he needs, a lung to breathe, eyes to see, etc. She explains that since they have harmed the Creeper, he is going to continue eating until he is not harmed anymore. She then says that one of the two has something he likes, but hes not sure which one yet. The way he finds out is by scaring you he can smell something in fear. It tells him if there is something inside a person that he might want. At this point, the lights in the police station go out and the emergency lights come on.
Darry doesnt understand how it is able to still be alive, since they ran over it so many times. Jez claims that he has eaten too many hearts for his own to stop. One of the cops heads to where the inmates are being held to get a head count. He approaches one cell where the two inmates are hovered against one wall in fright. On further inspection, the cop notices the Creepers clothing on the floor of the next cell, where the Creeper has eaten someone and is healing himself. The cop tries to shoot it but the Creeper overtakes him.
The cop with Trish, Darry and Jez tries to move them into a holding room after hearing the gunshots. Jez insists that they do not hide in room because she has seen the Creeper find them hiding in a room. She then says that she sees the song Jeepers Creepers playing on an old phonograph while one of them is screaming in the dark somewhere. The head cop then gets in a call saying that the Creeper is heading up the rear stairwell. He tells them all to stay where they are. After the cops leave, Jez says that she needs to get them out of there. They start running down one of the halls of the station.
We then hear over the radio that one inmate and an officer are down and then there are gunshots. He explains that they are unable to take him down, that he is wearing some kind of crazy armor. He then tells the sergeant that he is gone, heading up to the rest of the cops. Then the Creeper comes up behind one of the cops and punches a hole right through his stomach. They look up the staircase and see nothing, but hear something, so they begin shooting into the stairwell.
We then see that the way Jez tried to lead Trish and Darry out is locked. Trish argues with her and it comes out that she is there in the hopes that they can change the outcome. Darry figures out that she knows who it wants and what it wants. She explains that she has seen them run up the stairs and hide but that she doesnt know what happens. He asks her who hears Jeepers Creepers while screaming in the dark. Sobbing, Jez begins to look over at Trish. Darry asks if her dreams have never been wrong. She tells him that he doesnt understand. Trish, upset, says that Jez doesnt know anything. Then, the Creeper, comes out from around the corner. Jez yells for them to go upstairs.
The Creeper crawls over the wall and comes up behind Jez. He smells her and not finding anything he wants, he runs after Trish and Darry. In one of the interrogation rooms, Trish goes up to the two-way mirror and starts looking at her eyes. On the other side of the mirror, the Creeper is watching her and growling. The two are arguing when the Creeper smashes through the mirror. He picks up Trish and Darry up by their throats and proceeds to sniff them. He then licks Trish and after tasting her, he throws her to the side. He then licks Darry and seems to be pleased with the taste, when the cops from downstairs begin shooting one of the other two-way mirrors and aim their guns at the Creeper. They see that he has Darry in a headlock and do not shoot.
At this point, Trish runs up and tries to convince the Creeper that he wants her and not Darry. The Creeper then flies out the window with Darry in his arms. The next day, Trishs folks show up at the police station. Trish asks her what it means when Darry is screaming in the dark while the song is playing she wants to know what else she saw. Jez tells her that shes just a crazy old woman with crazy dreams and Trish walks out of the police station.
We then see an old factory where Darry is screaming and crying. In the background we hear the Jeepers Creepers song playing on an old phonograph. The Creeper seems to be sewing something together and we see that Darrys body is strung up and his eyes have been removed and the Creeper is using them as his own.