The film starts in February of 1979, at a steel plant in Lillian, Ohio. Elizabeth Lamb (Caitriona Balfe) has been killed in an accident. Though their family and friends are sad for her husband, Deputy Jackson Lamb (Kyle Chandler), their main concern is Joe Lamb (Joel Courtney), Elizabeth and Jackson's son. Joe was more attached to his Mom than his Dad, who was never really been there for his son.
Later at the Lamb's house, Louis Dainard (Ron Eldard) pays a visit. Jackson blames Louis for his wife's death, and forces him out of the house and puts him in his squad car. As Joe watches his father take Louis away, his gaze shifts to a silver locket in his hand.
Four months later, the local Middle School lets out for the summer. Joe's friend Charles (Riley Griffiths) has been shooting a Super 8 film for a film festival in Cleveland. Charles has rewritten the the story so that the detective now has a wife. Joe is unsure about this last-minute rewrite, but when Charles tells him that he has gotten Alice Dainard for the part (Elle Fanning), he becomes less-concerned. The two then promise to rendezvous later that night to film their scene, with plans for Alice to drive them.
Arriving home, Joe meets up with his Dad who takes him out for dinner. Jackson Lamb wants his son to attend a baseball camp for the summer, but Joe explains that he wants to help Charles finish his film. Both reach a impasse, having little more to say on the matter.
Later that evening, Joe goes to meet Charles and the rest of their crew: Cary (Ryan Lee), Preston (Zach Mills), and Martin (Gabriel Basso). When Alice shows up in her Dad's Buick Skylark, she's concerned that 'the Deputy's Son' knows she's driving without a license. Joe promises not to tell, and Alice reluctantly allows him along for the ride.
The group arrives at the Lillian Train Station, where Charles intends to shoot a scene with Martin as the detective of his story, trying to get his wife (aka Alice) to leave because of a zombie infection.
Joe is smitten with Alice, who shocks the guys when during the rehearsal, she delivers a performance that brings her to tears. The boys are snapped out of their shock by the sound of an approaching train. Charles demands they start filming again ASAP so they can put the train into their film and increase the 'production value.'
As they film the scene of the train thundering past the station, Joe catches sight of a white truck turning onto the tracks. The truck hits the train, causing a massive (and explosive) derailment. The gang runs for cover, and luckily survive the ordeal. Joe hears something pounding loudly on one of the derailed train cars right before the door flies off.
Surveying the wreckage, they come across some strange white cubes (Joe takes one), and find the wreckage of the truck. Inside, they find the body of one of their local science teacher, Dr Woodward (Glynn Turman). Joe removes a map from the doctor's hand. Everyone is shocked when he starts talking to them. Pulling a gun, he threatens them and tells them that they are not to tell anyone what they saw.
Suddenly, the sound of men approaching the wreck catches their attention. Fearful of being caught, they recover Charles' Super 8 camera, and quickly drive off. In the car, everyone is panicked about what just happened, and Alice says her coming was a mistake.
Analysis of the camera the next day reveals that it the lens is broken; however, Charles and Joe drop off the film for development. Joe insists he will help Charles finish the film, offering his Dad's video camera. However, Charles believes that Alice will most likely not want to help them after the night before.
Joe goes over to Alice's house to convince her to help them finish the film. Their conversation is interrupted by the arrival of Alice's father. He demands that Joe stay away from the family's home and Alice. Seeing that her father is somewhat drunk, she agrees to help Joe and his friends.
The gang then goes out to the scene of the train-crash, this time using it as background for their filming. During the filming, Joe notices that the train features Air Force insignia. Later at a restaurant, he peruses over the map that Dr Woodward had in his possession, noting a red line drawn in, snaking across the country. The group is still unsure why Woodward did what he did, but some are of the persuasion it was a failed suicide attempt.
Meanwhile, Jackson Lamb has come to the train-wreck site looking for answers. However, none of the clean-up crew or their superior, General Nelec (Noah Emmerich), are willing to tell him anything, other than the cargo and clean-up is not hazardous. Jackson notes the government men picking up strange little white cubes, and making plaster casts of some tire tracks in the ground.
The next day, the town devolves into a state of crisis, as Sheriff Pruitt (Brett Rice) goes missing. His wrecked vehicle is found near a gas station, with its windows smashed in and the attendant also missing. Jackson also receives reports of missing people, dogs and electrical equipment. While some report missing household items like microwaves, the oddest thing are missing electrical lines and engines straight out of vehicles!
Jackson soon grows concerned when the Military begins to roll into Lillian. Still not receiving answers as to their presence in the town, he receives word from one of the townspeople about a radio frequency that seems to be picking up Military transmissions. Jackson has the other officers tune their radios into the frequency, and soon hears word of something codenamed "Operation: Walking Distance."
Shortly after hearing the transmission, Jackson encounters Alice's father Louise, who tells Jackson to keep Joe away from Alice. Upset at hearing this, Jackson tracks down Joe, and takes back his movie camera as well. Jackson finds the Military moving stuff out of Dr Woodward's home. Finding General Nelec at the site, Jackson again demands answers. When he doesn't get any, he mentions 'Operation: Walking Distance.' This causes Nelec to agree to meet with Jackson later on that evening at a nearby airfield.
Taking him home, Jackson demands that Joe keep away from the Dainards, but Joe claims that Alice isn't like her father, and that she's nice. The two once again reach a wordless impasse, before Jackson storms out of the house. He then goes to the airfield to meet with General Nelec, only to be placed under arrest and locked away.
Joe heads over to the cemetery after this, where he sits at the headstone of his Mother's grave. While there, he hears some loud scraping and noises coming from a garage near the tombstones. Returning to his room later on, he is surprised when Alice appears. As they sit and talk, Alice asks Joe about the locket she's seen him carrying around. He claims it belonged to his Mother, and they retrieved it after her accident. Alice also finds Joe has a projector set up, and sees he has been watching home movies of his Mom from when he was younger. Alice tells Joe that she is sorry for the pain her Dad caused, and feels he really is not all bad. Joe tells that he also does not feel any ill will towards her Dad, when their attention is drawn to the strange white cube Joe picked up at the crash site. As they watch, it begins to vibrate, before shooting through a nearby wall, leaving a hole behind!
Alice then heads home, only to find her father drunk and smoking in their living room. Disgusted by her father's behavior, she rushes out and gets on her bike. Louis drunkenly follows in his car, but ends up crashing it. As Alice is unsure what to do, a she turns to see a large creature that causes her to scream. Louis attempts to get free of his wrecked car, but finds Alice and the creature gone!
The next day, Joe and Charles go to pick up the developed Super 8 film, but Charles is rather upset and cryptic towards Joe. When they finally get to Joe's place and watch the film, Charles explains that he is upset that Joe and Alice seem to be getting along and liking each other. The reason Charles cast Alice in the film, was because HE actually liked her. As they examine the film, their thoughts become turned when they see parts of a strange creature emerging from one of the wrecked train cars. As they wonder what it was they just saw, air raid sirens begin to go off.
They emerge outside to find the town being evacuated, with everyone being asked to report to the local Military base. Word is that a dangerous fire is headed towards Lillian, and could cause terrible damage if it reaches the town's chemical plant. Joe and Charles get on a bus, and are transported to the base. There, Charles is reunited with his family, while Joe goes to look for his Dad. However, he instead finds Louis, who tells Joe that he saw Alice being taken away by a creature, but nobody believes him.
Joe then rounds up Charles and their friends, with the intent to get back into town and rescue Alice. Bribing the town's camera-store owner to helping them, he manages to get them into town. They first go to the Middle School. Dr Woodward had a specially padlocked storage area behind the school where he hid confiscated items from his class. Joe assumes that there may be additional information as to his past, and the group finds numerous films, tapes, and records stored in there as well, that could help them find out more about the creature and how to possibly defeat it.
Breaking into the school, they use a film projector in one of the classrooms. Through the materials, they learn that the creature is sub-terranean, and mainly wants to just go home. However, General Nelec was more intent on keeping the creature for Army purposes. They also found its ship contained technology that when disassembled, 'shattered' into the little white cubes that the group saw at the crash site. Due to Woodward's interactions with the creature, he was able to gain a telepathic link to it, and notes in his findings that due to the hostilities directed towards it, it has grown hostile in nature to humans as well. The boys soon hear noises in the school, and are soon found by Nelec and his men. The group confiscate the items, as well as Joe's Mom's locket.
The boys are put on a Military bus and are headed back to the base when the creature attacks the bus. The boys manage to escape while the creature attacks the other Military Officers and kills General Nelec. In the aftermath, Joe is able to obtain his Mom's locket.
Meanwhile, Jackson has managed to escape his captors, and after creating a diversion, gets to the other base where the townspeople are being kept. He finds one of Joe's friends there, and after hearing of Joe's plans to rescue Alice, finds her father and takes him along. On their journey to the town, Louis explains that he came to the Lamb's house after the funeral to apologize. Jackson also admits that he knows that Louis is sorry, and quietly forgives him.
The boys meanwhile, have made it back into town, but suddenly find themselves in the middle of a war zone, as tanks and other Military weaponry are going haywire, firing random shots and destroying property. As the boys attempt to escape, Martin is injured. Charles stays behind to tend to his wounds, as Joe and Cary rush off to the cemetery.
Joe tells Cary about the strange things he saw and heard from the garage. Breaking down a door, they find a large hole, dug down several stories deep. Climbing down, they see it leads up into several other places. Eventually, they come across the creature's lair under the town's water tower, which houses all sorts of mechanical parts, including the missing items from the townspeople. As they watch, they see several people strung from the ceiling, including the missing Sheriff, as well as Alice! Before they can rescue her, they catch a glimpse of the creature, who is eating the limb of another human!
Fearful that Alice might be next, Joe directs Cary to create a distraction using the fireworks in his backpack. This causes the distraction that Joe needs as the creature heads down the tunnel towards the loud sounds. Joe manages to save Alice, as well as the Sheriff and a woman with rollers in her hair. As they rush to find a way out, they encounter Cary, who thought he was heading towards an exit. Suddenly, the creature comes up behind them, snatching the Sheriff and the other woman into the darkness.
Joe, Alice, and Cary run, but are soon at a dead end. The creature has them cornered, but Joe stands before it, reasoning with it. The creature acts hostile at first, but even in the face of its bizarre appearance, Joe does not react hostile like the previous treatment it has known. Suddenly, a sound is heard deep in the cave near the creature's lair, and it puts Joe down before returning.
The three return to the surface, and congregate near the water tower. As they do, all sorts of mechanical objects in the area become magnetized to the water tower's top area.Truck trailers nearby that also contained the recovered white cubes burst open, and the cubes begin to form around the edges of the water tower as well.
During the spectacle, Jackson and Louis come across their children, and both families reconcile as the creature ascends the watertower. As they watch, the locket in Joe's pocket attempts to fly away. Joe catches it, and we see what was inside it the whole time: a picture of Joe's Mom and him as a baby. Joe finally 'lets go' of his Mom, and the locket flies up to the magnetized watertower, where he metallic objects and the white cubes morph into a spaceship. The creature climbs aboard, as the top of the water tower disappears, raining down its watery contents on the people below.
Everyone watches as the ship ascends into the sky. As they do, Joe and Alice hold each other's hands. They and their families have reconciled over their past differences, but who knows what the future will bring?
*Extras over the Film Credits*
Over the film's credits, we see that Charles has completed his movie, titled 'The Case.' The Super 8 film consists of a detective investigating a rash of zombie appearances that seem linked to a company called 'Romero Chemicals.' The head of the company denies any wrong-doing, but the detective feels something is amiss. He attempts to send his wife away to keep her safe, but she refuses. While at the train station, they witness a train derailment (the footage captured on their camera replaced by model trains from Joe's collection). The detective soon encounters a doctor who has an antidote to the zombie disease, but only enough for one person. As he attempts to administer it to a captured zombie, the detective watches as the zombie bites into the doctor.
After killing the zombified Doctor, the detective returns home, only to find his wife has become a zombie! He stabs her in the neck with the antidote. It appears that it has not worked, and he prepares to kill his wife. However, suddenly she returns to normal, and the two embrace.
A final shot shows Charles in a suit and smoking a pipe, thanking the audience for watching, and considering them for the Cleveland film festival...before Alice pops into frame in her zombie make-up, 'terrorizing' the camera lens.