Life within the FAYZ, or Fallout Alley Youth Zone — the world beneath a dome that has children under 15 trapped in it without adults — continues to worsen. Now that Sam and Astrid have left the council, Edilio struggles to control the children still living in Perdido Beach. Everyone knows, however, that Albert, the boy in charge of rationing food and water, is really the one who runs things. Albert asks Sam to seek out a lake on the edge of the FAYZ because drinkable water is rapidly disappearing. Sam leaves in secret with Dekka and Jack so as not to cause a panic in town.
Drake, the reanimated villain with a deadly whip for an arm, escapes the prison Sam and others devised for him. Called by the gaiphage, Drake searches for the evil entity buried beneath the FAYZ. It also wants Drake to find Nemesis, the only power that can keep it from ruling the FAYZ.
Drake knows that he needs help controlling the other being that inhabits his body, a girl named Brittany. Brittany believes in a holy God and will try to stop the gaiphage’s plans. Drake wants revenge. Drake threatens a boy named Jamal with torture unless he keeps Brittany from ruining his plans.
Astrid has realized that her autistic brother, Little Pete, is the one who created the dome that keeps her and the other children trapped inside the FAYZ. Although she fiercely protects him, she begins to wonder whether his death would free them all. Meanwhile, a deadly flu strikes the town, causing some children to literally cough up their lungs and die.
The gaiphage creates carnivorous insects that bury themselves in their victim until the insect grows too big and must eat its way out. Then they continue growing. The insects hunt their prey in groups and then eat their victims alive.
Sam, Dekka and Jack encounter a horde of the creatures that they must fight. Dekka fears she has been infected by their venom and might have some growing within her. She begs Sam to kill her if they start to leave her body. They discover an abandoned military base where they also find a young boy named Toto. Scientists were studying him in the facility because he has the ability to know when people are telling the truth. Toto leads them to boxcars filled with soda, Nutella, small missiles and laptops. Sam and his friends indulge themselves before taking Toto with them to find the lake.
Lana, a girl with healing power, is unable to cure the flu-infected children. Sanjit, a newcomer to the town — helps her. Sanjit is attracted to Lana. His persistence eventually wins her over.
Caine, Diana and Bug remained on the well-stocked private island that formerly belonged to Sanjit’s celebrity adopted parents. Diana uses her sexuality to try and mellow Caine’s violent personality so he is not so power hungry and manipulative.
Drake is led by the gaiphage to a mineshaft where it is buried. Drake commands the carnivorous insects to remove the rubble that have held the gaiphage prisoner. The creatures rush to do his bidding. The creatures are hungry, so he allows them to eat Jamal. Even though the gaiphage demands Drake find Nemesis, Drake is driven with the desire to find the members of the council — especially Sam and Astrid — and kill them.
Sam and the others are thrilled when they find the lake and learn that the water is drinkable. Gas is also available from several marinas around the lake. It also has fish that the kids can eat. For once, Sam dreams of a happy future.
Little Pete has developed the deadly flu. To ease his fever, he blows off the roof of his house and creates rain. Orc, a boy who has been mutated to stone, sees the rain and investigates. Orc fears the council’s retribution because he accidently killed a child.
A gang of violent boys also sees the rain. They realize Pete must be creating it. They want to kidnap him so they can gain power within the FAYZ. Edilio arrives, and the boys tell him they have killed Albert. They threaten to kill Pete if the others try to stop them from taking him. Edilio shoots two of the boys, severely injuring them so they cannot hurt Astrid or Pete. Astrid asks Orc for help, and he carries Pete away from the house to the abandoned Coate’s Academy.
Ten miles below the earth’s crust, Brittany’s consciousness, not Drake’s, meets the gaiphage. The creature is a made up of billions of sand-like particles that live on the barrier below the earth. It keeps them trapped in FAYZ.
She cries out to God, but the gaiphage invades her mind, convincing her that it is an all-powerful creature from another universe, a god. It tells her that Nemesis must serve him so that it can leave this cocoon and live. She knows that Nemesis is Little Pete.
When Drake emerges, he is thrilled to learn the gaiphage desires he kill all those who will not serve it — all of Drake’s enemies. He sets off with half the insect army behind him to find Sam at the lake. After a violent battle, Sam, Dekka, Toto and Jack manage to escape and make their way back to the military base.
The bugs have infected Dekka, and they are beginning to eat their way out of her body. Using the last of her strength, she uses her powers to levitate the train car filled with missiles, with her friends on top of it, to Perdido Beach. When they crash into the ocean, Sam stays behind to try and keep Dekka alive as the insects leave her body. He sends Jack to find Little Pete, telling him to throw Pete to the insects, as it is the only way any of them will survive.
Edilio has the flu and believes Albert to be dead. He then learns that Drake is sending an army of mutant insects to town. Without Sam’s powers to protect them, Edilio makes the drastic decision to ask Caine for his help. Caine returns to Perdido Beach with Diana and his other followers. He insists that he be revered as a king before he will help them. They agree, calling him “Majesty” and bowing to him. But when the creatures attack, they soon overwhelm Caine. He barely survives the onslaught and must rely on another mutant for help.
After failing to kill Sam, Drake sets off to find Little Pete and Astrid. Astrid, though, is no longer near her brother. Orc fights to protect Pete until Astrid returns. Drake transforms into Brittany, and Orc throws her to the insect horde, but they do not attack her. Orc jumps down into their midst, intentionally trying to kill himself so the bugs will be distracted with him, allowing Astrid to escape.
Drake re-emerges, but Jack arrives before Drake can attack Astrid. As Drake and Jack fight, Astrid comes to the decision that it is better her brother die, and the FAYZ with it, than the gaiphage should be allowed to kill everyone who does not follow it. She throws her brother into the horde of insects.
Pete makes the insects disappear before vanishing himself. Drake transforms into Brittany, and she warns Astrid that the gaiphage will seek revenge on her for ruining his plan. Jack brings Astrid and the injured Orc to safety before Drake returns. He takes Astrid to Sam, where she confesses that she killed Pete. She becomes distraught when she realizes that it did not set them free and they remain within the FAYZ. She flees before anyone can console her.
Back in Perdido Beach, Caine takes credit for the disappearance of the insects and forces the survivors to bow to him. Several days later, the children of the FAYZ gather in the town center to make a decision. Those who remain in Perdido Beach will live with Caine as their king. Albert, who survived his brutal attack, will stay in town.
By doing so, he effectively stops Caine from becoming a dictator as every kid knows it is Albert who controls the distribution of food and water. Albert insists that Toto remain in town as well, as his gift of being a human lie detector will prevent Caine from being too dishonest. Sam is surprised when Diana asks to join him and his group who are going to live up by the lake. She confesses to him that she is pregnant with Caine’s baby and does not want him to know. Astrid never comes back, and Sam, reluctantly, leaves without her.
The novel ends from Little Pete’s perspective. He has left his body behind, but his consciousness is free n some other realm. He can see the Darkness also called the gaiphage below him, but knows it is afraid of him. He enjoys the sensation of being alive, without the constraints of his autistic brain and sick body.