Sigma, who has been revived again (as in X4, it is unknown who revived him or how), conducts research on the origin and design of Zero and decides to discover how to unlock Zero's true power, hopefully destroying X in the process. Sigma attacks the Maverick Hunters directly, intending to lose. When he does, he spreads the Maverick virus across the Earth, throwing it into chaos. Meanwhile, a Reploid mercenary named Dynamo is hired by Sigma to make the space colony Eurasia collide with Earth. The Hunters have only 16 hours to stop the collision.
In order to prevent Eurasia from striking the planet, the Hunters pursue two options. The first option is to fire a powerful cannon called Enigma at Eurasia, vaporizing it. If the Enigma shot fails, the second option is to launch a space shuttle and pilot it into the colony, destroying it. To maximize their chances, X and Zero are dispatched to collect parts for the two devices. The necessary parts to upgrade the Enigma and shuttle are held by eightReploids and Mavericks), and X and Zero must defeat them to claim the parts.
Whether the Enigma and shuttle succeed or fail is randomly determined by the game, although the Enigma's chances of working successfully are low even with all its parts, while the shuttle has a much higher probability of succeeding assuming all of the parts are collected. Whether the Enigma succeeds or fails, a "new" virus appears on the Earth, noted by Alia as the Sigma virus combining with the scraps from the colony. If the Enigma or the shuttle succeeds, X and Zero proceed to hunt for the cause of the virus. If the shuttle fails or if the time expires, the colony crashes, nearly destroying the planet; Zero then is infected by the virus and goes Maverick.
In either case, once the location of the virus' origin is discovered, the Hunters investigate. X and Zero penetrate a bizarre underground fortress. In the fortress, X and Zero cross paths, where mutual suspicion and mistrust leads to a duel between the heroes (which had been foreshadowed since the end of Mega Man X3).
After the duel, the story diverges slightly. If Zero went Maverick, he sacrifices himself to save X from Sigma, and X continues on alone to defeat Sigma. If Zero did not go Maverick, he saves X and himself from Sigma, and both have a chance to confront Sigma.
There are three possible endings. If Zero went Maverick, X defeats Sigma, but is badly damaged. A mysterious figure recovers him, but also deletes all his memories of Zero. X is seen, three years later, talking to two other hunters, while Douglas, Alia, and Signas discuss the fact that X's memory of Zero has been deleted. This ending is treated as non-canon by Capcom, as there are further games where X and Zero work together.
If Zero did not go Maverick, Sigma decides to make the Hunters' victory for naught by taking them down with him. X tries to save Zero but is ambushed by Sigma and both Hunters are critically damaged. Zero manages to finish Sigma off, then the endings diverge again. If Zero defeated Sigma, he reflects on his origin and life before dying. If X defeated Sigma, he inherits Zero's beam saber and continues to fight as a Maverick Hunter. This is considered the "true" ending.
In each of X's endings, the mysterious figure is shown to be a hologram of Dr. Light, who discovers X's badly damaged body after the battle with Sigma and repairs X, saying "Not yet... Actually, I want you to rest and relax for now. Hold on X... Just for a few more moments."
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