This follows the story of John Smith, a 15-year-old alien from the planet Lorien, and Henri, his guardian Cêpan, as they run from the Mogadorians, another alien race that is hunting John and eight other teenage Lorics residing on the planet Earth. These nine teens are members of the Garde, a group of Loric people gifted with special powers called "Legacies." Cêpans, who are also Loric, do not acquire legacies and most often become protectors and mentors for young members of the Garde. The teenagers are protected by a spell or charm that only allows them to be killed in numeric order. The first three have been killed, and John is Number Four.
The book opens with the death of Number Three. Number Four is introduced under the alias Daniel Jones as he leaves Florida. Four has three circular scars which begin on his right outer leg, just above his ankle, and move upward along his outer calf. Each signifies the deaths of Numbers One, Two, and Three, and burn with blue fire when they appear. These scars are present on all the Lorien teenagers, and with each death, another scar appears. Henri, Four's Cêpan (guardian), tells him they are going to Paradise, Ohio. Henri produces a new identity for Four, giving him the name "John Smith."
Tired of running, John says that he wants to begin to make a life for himself. Henri reminds him why they run, and the conversation ends. John begins to attend the local high school where he meets the beautiful Sarah Hart, a junior. He also meets her ex-boyfriend Mark James, who immediately begins to pick on John. John stands up to him, the first time he has ever stood up to anybody.
During astronomy class, John's hands begin to hurt and glow. When John is back at his house, he realizes that his first legacy has arrived. After the Mogadorians' devastating attack on Lorien, the Nine are the only surviving Lorics with legacies - and each of the Nine is gifted with a different set of legacies (though they all have telekinetic powers). Henri tells John that his first legacy is Lumen, the ability to produce light from his hands, accompanied by a developing resistance to fire. Henri uses an oblong milky white stone to help John spread his resistance to fire and heat throughout his body. During this process John sees a vision of his last moments on Lorien when the Mogadorians attacked, while Henri narrates.
Henri and John have a special Loric chest that can only be opened by both of them together. (However, if Henri dies, John will be able to open it by himself.) Using artifacts from the chest Henri shows John a model of the galaxies where he can see how Lorien looked before the Mogadorians destroyed it and how it looks now, desolate and barren. The chest also contains a healing stone that heals all wounds inflicted on the body, but with conditions: the healing process is twice as painful as the injury itself, and the wound must have been inflicted with intent to harm. The stone must be used soon after the injury occurs. Also in the chest are several small pebble-like rocks, Lorien salt, that can be placed under the tongue for a burst of strength and relief from pain. The effects of the salt are rapidly diminished by the use of legacies.
With the arrival of John's legacies, Henri begins to train him. John eventually learns to turn his lights on and off at will. John also makes his first real friend, Sam Goode, who believes in aliens. He also grows closer to Sarah. At a town Halloween party John, Sarah, Sam, and Sarah's friend Emily are ambushed by Mark and some of his football teammates. John, who is already tired of Mark's constant bullying, is enraged when they run off into the woods with Sarah. John chases the boys and finally confronts Mark and his friends, easily defeating all of them and freeing Sarah. Sam witnesses much of the ordeal and becomes wary of John, avoiding him for some time.
When John goes to Sam's house to talk to him, he threatens John with a gun but John convinces him he's not an alien so he leaves with a magazine on alien conspiracies. John is invited to a dinner at Sarah's house. Henri has gone to Athens, Ohio because he discovers an alien conspiracy magazine and goes to find out how they had gained information on mogadorians and hasn't called John yet like he promised. So John calls Sam for help. Sams drives John to Athens, where they find Henri ambushed and captured inside the publisher's house. John's telekinesis legacy appears, and he uses it to save both Henri and Sam and escape the house as several Mogadorian scouts arrive. Henri tells Sam their whole story, and after seeing John use his telekinesis Sam accepts them for who they are. John's training intensifies until he is able to perform complex telekinetic feats with his clothes lit on fire.
At a party at Mark's house, a fire starts, trapping Sarah on the second floor. John rushes in and saves her, revealing who and what he really is to her in the process. She still confesses her love for him, and John says he loves her too. He then proceeds to tells her everything about himself. At school the next day, John fears that he will have to leave, as people had seen him jump out of the window and reported it. Fortunately, the paper has no reference to his involvement in the fire. All seems to be going well when a fax arrives for John at the school saying "Are you Number Four?" John leaps through a window and rushes home to find Mark, who has realized the truth. He argues with Henri about why he did what he did, saying he wanted a normal life. He then frantically returns to the school to find Sarah when he realizes that the Mogadorians are on their way.
John finds Sarah, but they encounter a Mogadorian scout, one of several who have closed in on the school. John kills it, but their escape route is blocked by two more Mogadorians until Henri and Mark arrive and kill the scouts. The four are then joined by a girl about John's age and John's dog, Bernie Kosar. The girl identifies herself as Number Six. John realizes that since he and Six have met, the charm protecting them from being killed out of order has now broken. Six replies that the war has begun and that they must fight. While the five companions make their way out of the school, John tells Mark and Sarah to go back and hide, as it isn't their fight. They do, and in the battle that ensues John confronts his first soldier, whom he kills.
John is wounded severely and is rescued by Henri as well as Sam, who realized what was happening and has come to help. John discovers his third legacy, the ability to communicate with animals and also finds out that bernie kosar is an chimaera, and convinces one of the Mogadorians' beasts to turn on its masters. In the chaos Henri is hit by a Mogadorian's energy blast and dies in John's arms. Before he passes away, he says, "Coming here, to Paradise, it wasn't by chance."
Waking up in a hotel room, John tells Sarah that he has to leave. Sarah accepts this and tells him she will wait for him. John replies in a similar fashion, saying his heart will always belong to her. Afterward, Henri's body is cremated. Sam agrees to go with John and Six as they prepare to leave in search of the other four Loric children. The novel ends with John telling Sarah he loves her and will come back and then he's leaving with Six, Sam and Bernie Kosar.
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