Young Jodie Holmes (Caroline Wolfson) lives on a military base with her foster parents. Since birth, Jodie has possessed a psychic connection with a mysterious entity named Aiden, through whom she can perform telepathic acts, such as possessing peoples' minds and manipulating certain objects. After an incident with some neighbourhood kids results in Aiden almost killing them, Jodie's foster parents seek help to care for her condition, permanently leaving her under the custody of doctors Nathan Dawkins (Willem Dafoe) and Cole Freeman (Kadeem Hardison) of the fictional United States Department of Paranormal Activity.
Under the two doctors' care, Jodie slowly learns to control Aiden and the powers they share. During this time, Nathan and Cole are building the condenser, a portal which connects the world of the living with the world of the dead—the Infraworld. One night, Nathan learns that his wife and daughter were killed in a car accident. While trying to comfort him, Jodie discovers that she can channel spirits of the dead from the Infraworld; she helps the spirits speak to the living through a psychic link created by her physical contact. As the years pass, a teenage Jodie (Ellen Page) seeks her independence, both from the doctors and from Aiden, and tries several times to live a normal life. At each attempt, Aiden intervenes, ending in disaster.
At one point, Nathan asks for Jodie's help with the condenser, which has broken open. After braving hostile entities, Jodie manages to shut down the condenser and warns Nathan not to build another. This gets the attention of the CIA, who send agent Ryan Clayton (Eric Winter) to forcibly recruit Jodie. After weeks of training, now-adult Jodie goes on multiple missions as a field agent, often with Ryan, to whom she slowly becomes attracted. On one such mission in Somalia, Jodie learns that the target she killed was not a warlord, but the country's benign president. An enraged Jodie flees in disgust, despite Ryan's pleas. Branded a traitor, Jodie becomes a fugitive, evading and fighting pursuing CIA forces. Along the way, she befriends a group of homeless people, one of whom she helps give birth to an infant named Zoey, and a family of Native Americans whom she saves from a malevolent entity. The CIA eventually recaptures Jodie while she attempts to reconnect with her catatonic biological mother, held and forcibly drugged for decades in a military hospital.
The CIA hands Jodie over to Nathan, now executive director of the DPA, overseeing the DPA's newest condenser, code-named the Black Sun. He reveals that the CIA is willing to let Jodie go if she agrees to a final mission. Jodie and a CIA team led by Ryan destroy a facility housing a Chinese-developed condenser before it is used to attack the United States. Jodie then learns that Nathan built a miniaturized condenser to speak exclusively to his family, but without success. After showing Nathan that his refusal to let them go are only making them suffer, Jodie tries to leave, only to be held in captivity by the CIA—the organisation has deemed her too dangerous to be freed. Jodie is subjected to the same fate as her mother. Nathan appears and informs Jodie that he's decided to shut down the containment field to the Black Sun, merging the two worlds together and making death meaningless. Too weak to free Jodie, Aiden contacts Ryan and Cole, leading them to her. After Nathan shuts down the containment field, the three chase after him into the heart of the Black Sun, with the intent of destroying it.
During the trek towards the Black Sun, Cole is injured by entities, and Ryan sacrifices his own safety to keep Jodie alive. Eventually, Jodie confronts Nathan near the Black Sun. He commits suicide to reunite with his family. As Jodie shuts down the condenser, she has a vision—Aiden is her stillborn twin brother. Jodie must make a choice: go back to the world of the living, or go on to the Infraworld and be reunited with everyone she has lost. By the story's end, the Infraworld has become a widespread threat in the not-so-distant future. Accompanied by the now-teenage Zoey, Jodie prepares to confront the threat.
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