After seven months inside the dome known as the FAYZ, life is getting grim. Although Sam, Astrid and the other members of the council try to keep order; graffiti, substance abuse and violence are becoming more common. Astrid wants to make council rule the law inside the FAYZ, but when problems arise, the children call on Sam to solve them instead of the council.
Zil and his followers don’t want Sam or any of the other “freaks” to be in charge of the FAYZ. Freaks are kids with special powers like Sam, who can throw lightning from his hands. Other freaks can move very fast, transport themselves from one place to another or levitate things. Zil and his gang kidnap any freaks they find and force them to live away from “normal” human kids.
Meanwhile, Nerezza, a mysterious girl whom no one can remember from before the FAYZ, has labeled Orsay, a girl who can see other people’s dreams, a prophetess. Orsay claims to be able to contact parents outside the dome. She insists that when they turn 15, they should embrace the “poof,” which is when children disappear from the FAYZ unless they fight against it.
Orsay believes they will be reunited with their parents outside of the dome. Astrid believes that to willingly poof will lead to their death. Sam keeps secret the fact that a girl named Brittany appears to have clawed out of her grave and is now alive again. Brittany hears a voice speaking to her, encouraging her to be good. However, another presence inside her is evil. She often loses time and is unaware of what she’s doing.
Caine, Sam’s twin brother and the leader of the remaining students from the Coates Academy, is barely alive. He and his handful of followers have resorted to cannibalism in order to survive. One of his gang, a boy named Bug, believes there might be food on one of the islands just offshore of Perdido Beach. He knows that a famous movie star couple lived on one of them, and he figures they must have stocked it with lots of food.
Bug is correct in believing there is food there, but the five adopted children of the movie stars are rationing it. Sanjit, a 14-year-old Hindu boy, tries to keep his siblings calm and fed. Virtue, or “Choo,” the next oldest, is worried about their younger brother, Bowie. He has been sick with a very bad flu. Choo tries to convince Sanjit that he should use the helicopter to fly them to shore so they can find help.
Astrid hears a rumor that another boy, Drake, has also returned from the dead. Drake had terrorized the town, controlled by an evil force known as the gaiaphage. Drake used his mutant whip arm to slash his victims. Sam had barely survived when Drake attacked him. The psychological terror still affects him. Edilio, a member of the Council and head of the police force, finds a body that has been brutally murdered. There is no doubt Drake did it. Sam struggles to keep himself together at the possibility of having to face his nemesis again.
Mary, the girl in charge of the town’s day care, is falling apart. Anorexic, bulimic and suffering from depression, she survives on what antidepressants she can scavenge from Dahra, the girl in charge of medicine. As she nears her 15th birthday, Orsay prophesizes that Mary should free the children and go home. She says that Mary will lead the children to freedom as a red sun sets on Mother’s Day, her birthday.
Caine convinces Zil to attack the freaks of Perdido Beach. Zil and his gang make Molotov cocktails and throw them into houses inhabited by freaks. Caine is hoping the distraction will keep Sam from the marina so he can steal a boat without resistance. Zil agreed to the plan because he hopes to turn the rest of the “normal” kids to his side so he can rule inside the FAYZ. Some of Zil’s gang begin shooting at children as they run for help. Caine escapes with a boat. Sam searches for Zil, but encounters the undead Drake. Terrified, Sam flees the town.
Lana, a girl with healing powers, returns in order to help the kids burned by the fire. She has been living apart since she had been connected mentally to the gaiaphage. She, Sam and the other members of the council had hoped the creature had been destroyed, but she knows it lives. She believes the gaiaphage is still using her powers. She also warns Mary that the council might not be what it seems. She knows they have been lying about Orsay, Drake and Brittany. She wonders if they really want the dome to be destroyed or if they enjoy being the “rulers” of those inside the FAYZ.
Mary figures out that if the gaiaphage is still alive, it must have used Lana’s powers to bring Drake and Brittany back to life. The next day, Astrid tries to maintain control of the council, but all semblance of order falls apart. She knows she has lost any authority she once had and so leaves the meeting with her little brother, Petey.
Caine and his minions manage to get to the island. They find Sanjit and Choo, who try to convince them that they are lepers. Their ruse does not work but only incites Caine to mistrust them. The boys take the Coates students to their mansion and lace their food with sleeping pills. Caine and the others pass out. Sanjit agrees to try to fly his siblings off the island.
The kids in town gather for a barbecue. Astrid uses the opportunity to talk to them once more. This time she’s made a list of 10 rules for them all to vote on about how the FAYZ should be run. She admits she lied to people about what was happening in the FAYZ; once the rules are voted on, she quits the council.
As most of the kids are eating, Nerezza shows up and convinces Zil that darkness is coming and he needs to get his weapons and begin killing. At the same time, Mary runs from the day care. She screams that Drake is inside. Edilio takes aim at the next person exiting, but it is Brittany, not Drake. She claims that the demon is near.
Nerezza approaches Mary and tells her to take the children to safety. She must get them to the cliff above the beach. Chaos ensues as Zil and his gang start to shoot at any freaks they find in the square. Brittany morphs into Drake, creating even more havoc. Astrid realizes that the gaiaphage and Petey are locked in a battle through Petey’s video game. Nerezza is the gaiaphage’s evil pawn. Petey, unknowingly, is fighting for good.
Sanjit and his siblings get to the helicopter, but Caine arrives in time to use his powers to keep them from flying away. His girlfriend, Diana, begs him to let the children go, but he is unwilling. Another girl, Penny, goads him to kill them by claiming Diana makes him weak. Caine levitates Penny above the copter’s rotor blades to shut her up.
Diana backs herself up toward the cliff, threatening to kill herself if Caine insists on hurting the children. She accidently falls over. Caine uses his power to keep her from plummeting to her death, but loses his grip on Penny. She falls to the rocks below. He also loses his hold on the helicopter so that Sanjit can fly away. They eventually crash safely onto Perdido Beach.
Zil and his gang continue to hunt down freaks. All the children race toward the beach. Dekka, a freak who can control the wind, tries to stop Zil. He and his minions shoot at her, but she keeps up her attack. She grabs Zil, lifting him high into a whirlwind. When Zil tries to shoot her with his shotgun, the recoil loosens her hold on him, and he falls to the ground.
Mary leads the children to the cliff and then, on Nerezza’s urging, has them join hands with her and pulls them off the side. Several freaks use their powers to keep the kids from dying on the rocks below. Brittany, now morphed into Drake, attacks Astrid. Sam arrives to fight him again, but is stopped when Nerezza orders a freak named Jill to sing.
Jill’s singing incapacitates those who hear it. Luckily, the sound of Sanjit’s helicopter drowns out her voice and Sam continues fighting. Drake transforms back into Brittany. She begs Sam to kill the demon within her, but instead, he chains her up. Petey’s game is broken. As he pitches a fit, the walls of the FAYZ disappear, and Astrid catches a glimpse of crowds of people and satellite trucks. The wall comes back when Petey stops screaming.
Sam and the council keep the Drake/Brittany creature locked up in a basement. Order returns to the FAYZ, but they all know how close they came to being defeated by the machinations of the gaiaphage. No one knows whether the brief glimpse of the world outside the FAYZ was real, but Sam hopes no one realizes how Petey seems to be in control of the dome. He fears that someone besides the gaiaphage will try to kill the boy if his secret is discovered.