MGM had originally planned to release the movie direct to DVD, but was unable to find proper financing. In 2006, the film was officially announced and was tentatively called Jeepers Creepers 3: The Creeper Walks Among Us. The third film was in development before Jeepers Creepers 2 was released in 2003.
Gina Philips as Trisha "Trish" Jenner (cameo).Gabrielle Haugh as Addison "Addi" Brandon.Twenty-three years later, Trish Jenner is seen reading an open letter she presumably wrote on a computer calling for people to fight against the Creeper when it returns and vows to get revenge on The Creeper for the death of her brother, Darry. The next day, Addison says goodbye to Buddy before he leaves for a high school basketball game in the same bus that is attacked by the Creeper before its hibernation. The Creeper returns to Gaylen's house where he finds a sign that says 'We know what you are', along with the hand, and howls in anger. Addison hides in a field where she is found by Gaylen and Buddy.
When the truck driver gets out to see what happened, he is killed and his body was used by the Creeper to heal itself. He is hit by a truck and Addison runs away. She escapes as the Creeper loses an eye he tries using his weapons to kill her but his aim is off. That night, the Creeper discovers that Addison is still alive, but before he can kill her, she causes the metal pipe to shoot out and impale his head. With most of the team gone, Tubbs retreats. Tashtego shoots him many times but the bullets have little effect and he is struck in the head with an axe. Before the Creeper can kill Tubbs, Tashtego yells for its attention seeming to sense he knows about it, the Creeper leaps after him. A small explosive is ejected from the Creeper's truck and Tashtego and Tubbs' car lands in a field. They find the Creeper driving down the highway, but when they shoot at it, the bullets deflect and Michael is killed. Tashtego and Tubbs discover the Creeper's location and they head off, along with Michael. Addison wakes up in the Creeper's truck with Kirk Kirk accidentally activates a booby trap, causing a metal pipe to impale his head. When Tashtego's team arrives, Gaylen reveals the hand can tell them about the Creeper Tashtego touches the hand, left shocked by how ancient the Creeper is. Gaylen digs up the hand Kenny found she touches it, going into a trance.
They find the owner and workers hiding under cars the owner tells them to call for help. Addison goes into town to buy hay for her horse and joins her friend Buddy in delivering hay to a plantation house.
As the other boys try to free him, the Creeper kills them all. A group of teenagers discover the Creeper's truck in a field one of them, Kirk, accidentally activates the spear, getting impaled in the leg. Tubbs joins a small team Tashtego put together from relatives of Creeper victims to kill it. The next day, Kenny Brandon's mother Gaylen sees a vision of Kenny, who was killed by the Creeper he warns it will come for what he buried on the property and will kill her and his niece Addison. As Frank and Deputy Lang transport the vehicle, the Creeper abducts Frank. They rush to get the Creeper's truck back after learning it is headed for the impound. When Sheriff Dan Tashtego arrives, he informs Sergeant Davis Tubbs of the Creeper and its motives. A day after the events of the first film, the police discover the Creeper's truck filled with dead bodies however, the truck is booby-trapped with spikes.