In 1979, Deputy Sheriff Jack Lamb of Lillian, Ohio, and his 14-year-old son Joe, mourn wife and mother Elizabeth, killed in a workplace accident. Jack blames Louis Dainard, whose shift she was covering as he showed up drunk. All Joe has left of her is a locket.
Four months later Joe's friend Charles is making a zombie movie for a Super 8 film competition. He enlists Joe's help along with friends Preston, Martin, and Cary, as well as Dainard's daughter, Alice. Though their fathers would be furious, Joe and Alice become close.
While filming at a train depot at midnight, a train approaches and a pickup truck rams the train head-on, derailing it and destroying the depot. The children are separated in the chaos. Joe sees the door of a train wagon violently thrown off. The kids regroup and find crates of strange white cubes amid the wreckage before discovering the truck driver to be their biology teacher Dr. Woodward. Barely alive, he warns them at gunpoint to forget what they have seen. They flee as a convoy from the local Air Force base, led by Col. Nelec, arrives. Nelec finds an empty super 8 film box.
In the following days the town experiences strange events; the dogs run away, several townspeople go missing, the electrical power fluctuates, and electronic items are stolen. Sheriff Lamb approaches Nelec but Nelec has him arrested and orders flamethrowers to start a wildfire as an excuse to evacuate the residents to the base. Joe and Charles watch their derailment footage and see that a large creature escaped the train. Nelec confronts Woodward in a military hospital for information about the creature, but when Woodward rebukes him, Nelec has him killed.
Alice's father tells Joe the creature has abducted her. Joe, Charles, Martin, and Cary persuade Jen, Charles' older sister, to flirt with Donny so he can get them into town to rescue Alice. Breaking into Dr. Woodward's trailer they find documents and a film from his time as a government researcher.
The film reveals the Air Force captured an alien when it crash-landed in 1958, and experimented on it while withholding its ship composed of the strange white cubes, allowing it to shape-shift. The alien had established a psychic connection with Woodward, who sought to help it escape Earth, but Nelec sabotaged, discredited, and discharged Woodward. Nelec captures the kids but the alien kills Nelec and the airmen, allowing the kids to escape. Lamb escapes and agrees with Dainard to put their differences aside to save their kids.
The military attacks the alien but their hardware goes haywire in its presence, resulting in significant collateral damage. Joe and Cary find a massive tunnel system under the town. The missing townfolk, including Alice, are hanging unconscious from the ceiling of a cavern where the alien is creating a device from the stolen electronics attached to the base of the water tower. Using firecrackers as a distraction, Joe frees Alice and the others. The alien grabs Joe, who quietly speaks to it, saying "bad things happen" but that it "can still live". The alien allows them to return to the surface.
Everyone watches as metal objects from all over town are pulled to the top of the tower by an unknown force. The white cubes reassemble as the spaceship and, as the alien enters it, the locket in Joe's pocket is drawn toward the tower. After a moment, he lets it go, completing the ship. As the ship rises into space, Joe takes Alice's hand.
The detective-zombie short film the children were making in Super 8 rolls runs at the end of the movie beside the credit roll. In it, Charles asks for his short film "The Case" to be picked for a local film festival before being attacked by Alice as a zombie.
Joel Courtney as Joe Lamb
Elle Fanning as Alice Dainard
Riley Griffiths as Charles Kaznyk
Ryan Lee as Cary McCarthy
Gabriel Basso as Martin Read
Zach Mills as Preston Scott
Kyle Chandler as Deputy Jackson Lamb
Ron Eldard as Louis Dainard
AJ Michalka as Jen Kaznyk
Joel McKinnon Miller as Sal Kaznyk
Jessica Tuck as Mrs. Kaznyk
Brett Rice as Sheriff Pruitt
Michael Giacchino as Deputy Crawford
Michael Hitchcock as Deputy Rosko
Jay Scully as Deputy Skadden
Noah Emmerich as Colonel Nelec
Richard T. Jones as Overmyer
Bruce Greenwood as Cooper
David Gallagher as Donny
Glynn Turman as Dr. Thomas Woodward
Beau Knapp as Breen
Dan Castellaneta as Izzy
Caitriona Balfe as Elizabeth Lamb
Dale Dickey as Edie