After completing his training, UNATCO agent JC Denton takes several missions given by Director Joseph Manderley to track down members of the National Secessionist Forces (NSF) and their stolen shipments of the Ambrosia vaccine, the treatment for the Gray Death virus. Through these missions, JC is reunited with his brother, Paul, who is also nano-augmented. JC tracks the Ambrosia shipment to a private terminal at LaGuardia Airport. Paul meets JC outside the plane and explains that he has defected from UNATCO and is working with the NSF after learning that the Gray Death is a human-made virus, with UNATCO using its power to make sure only the elite receive the vaccine.[28]

JC returns to UNATCO headquarters and is told by Manderley that both he and Paul have been outfitted with a 24-hour kill switch and that Paul's has been activated due to his betrayal. Manderley orders JC to fly to Hong Kong to eliminate Tracer Tong, a hacker whom Paul has contact with, and who can disable the kill switches. Instead, JC returns to Paul's apartment to find Paul hiding inside. Paul further explains his defection and encourages JC to also defect by sending out a distress call to alert the NSF's allies. Upon doing so, JC becomes a wanted man by UNATCO, and his kill switch is activated by Federal Emergency Management Agency (FEMA) Director Walton Simons. JC is unable to escape UNATCO forces, and both he and Paul (provided he survived the raid on the apartment) are taken to a secret prison below UNATCO headquarters. An entity named "Daedalus" contacts JC and informs him that the prison is part of Majestic 12, and arranges for him and Paul to escape. The two flee to Hong Kong to meet with Tong, who deactivates their kill switches. Tong requests that JC infiltrate the VersaLife building. Doing so, JC discovers that the corporation is the source for the Gray Death, and he can steal the plans for the virus and destroy the universal constructor (UC) that produces it.[29]

Analysis of the virus shows that its structure was designed by the Illuminati, prompting Tong to send JC to Paris to obtain their help fighting Majestic 12. JC meets with Illuminati leader Morgan Everett and learns that the technology behind the Gray Death was intended to be used for augmentation, but Majestic 12, led by trillionaire businessman and former Illuminatus Bob Page, stole and repurposed it. Everett recognizes that without VersaLife's UC, Majestic 12 can no longer create the virus, and will likely target Vandenberg Air Force Base, where X-51, a group of former Area 51 scientists, have built another one. After aiding the base personnel in repelling a Majestic 12 attack, JC meets X-51 leader Gary Savage, who reveals that Daedalus is an artificial intelligence (AI) borne out of the ECHELON program.

Everett attempts to gain control over Majestic 12's communications network by releasing Daedalus onto the U.S. military networks, but Page counters by releasing his own AI, Icarus. Icarus merges with Daedalus to form a new AI, Helios, which can control all global communications. Savage enlists JC's help in procuring schematics for reconstructing components for the UC that were damaged during Majestic 12's raid of Vandenberg. JC finds the schematics and transmits them to Savage. Page intercepts the transmission and targets a nuclear missile at Vandenberg to ensure that Area 51, now Majestic 12's headquarters, will be the only location in the world with an operational UC. However, JC can reprogram the missile to strike Area 51.

JC travels to Area 51 to confront Page. Page reveals that he seeks to merge with Helios and gain full control over nanotechnology. JC is contacted by Tong, Everett, and the Helios AI simultaneously. All three factions ask for his help in defeating Page while furthering their own objectives. Tong seeks to plunge the world into a Dark Age by destroying the global communications hub and preventing anyone from taking control of the world.[30] Everett offers Denton the chance to return the Illuminati to power by killing Page and using the Area 51 technology to rule the world with an invisible hand.[31] Helios wishes to merge with Denton and rule the world as a benevolent dictator with infinite knowledge and reason.[32] The player's decision determines the future and brings the game to a close.

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