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In the past, an intellectual race called the Forerunners fought an alien parasite known as the Flood. The Flood, which spread through infestation of sentient life, overran much of the Milky Way Galaxy. The Forerunners conceived a weapon of last resort to combat the Flood. Using an installation known as the Ark, they built large ring-shaped megastructures known as Halos. The Halo Array, when activated, would destroy all sentient life in the galaxy—depriving the Flood of their food. Delaying as long as they could, the Forerunners activated the rings and disappeared.

Tens of thousands of years later in the 26th century, humanity—under the auspices of the United Nations Space Command or UNSC—colonize many worlds thanks to the development of faster-than-light "slipspace" travel. Tensions escalate between the older and more stable "Inner Colonies" and the remote "Outer Colonies", leading to civil war. The UNSC creates an elite group of enhanced supersoldiers, known as Spartans, to suppress the rebellion covertly. In the year 2525 the human colony of Harvest falls under attack by a theocratic alliance of alien races known as the Covenant. The Covenant leadership declares humanity heretics and an affront to their gods—the Forerunners—and begins a holy war of genocide. The Covenant's superior technology and numbers prove decisive advantages; though effective, the Spartans are too few in number to turn the tide of battle in humanity's favor.

In 2552, the Covenant arrive at Reach, the UNSC's last major stronghold beyond Earth, and launch an invasion of the planet. The last Spartans and UNSC military are unable to stop the Covenant from bombarding the surface with plasma. Following directives to avoid leading the Covenant to Earth, the artificial intelligence (AI) Cortana aboard the fleeing UNSC ship Pillar of Autumn selects random coordinates that lead the ship to a Halo installation. The Covenant follow, damaging the Autumn and leading its crew to take the fight to the ring's surface. The Covenant accidentally release Flood imprisoned on the ring; in order to nullify the threat, the ring's AI caretaker, 343 Guilty Spark, enlists the help of the Spartan, John-117. Before the pair can activate Halo's defenses, however, Cortana reveals that Halo's activation would mean their own destruction. Master Chief and Cortana instead detonate the Autumn's engines, destroying Halo and preventing the escape of the Flood. They and a few other human survivors return to Earth, warning of an impending Covenant attack.

Soon after, a Covenant fleet arrives at Earth. Most of the fleet is destroyed, but a single ship under the command of one of the Covenant's Hierarchs, the Prophet of Regret, breaks through the human defenses and invades the African city of New Mombasa. Before the humans can assault Regret's carrier, he retreats through a slipspace portal, pursued by the Master Chief aboard the human ship In Amber Clad. Regret travels to another Halo installation, where the Master Chief kills Regret. Inner turmoil in the Covenant leads to civil war between the various member races. Learning that the activation of the Halo Array (a central tenet of the Covenant religion) would lead to their extinction, the Covenant warrior Arbiter and his brethren ally with humanity to stop the rings from being fired. The aborted activation of the ring puts all the Halo installations on standby: the remaining rings can be activated remotely from a location known as "The Ark".

The Covenant begin a full-scale invasion of Earth and excavate a Forerunner artifact in the African desert that creates a slipspace portal to the Ark. The Master Chief and Arbiter travel through the portal to kill the last High Prophet, Truth, and discover the installation is building a new Halo ring to replace the one destroyed previously. In order to destroy the spreading infestation led by the Flood intelligence Gravemind, the Master Chief activates the incomplete ring—as the Ark lies outside the Milky Way Galaxy, the blast destroys the Flood but spares the galaxy at large. Because the ring's construction is incomplete, the resulting pulse destroys the ring and damages the Ark. The Arbiter escapes the explosion through a slipspace portal, but only half the ship makes it through before it closes. The Master Chief and Cortana are left drifting in space, trapped in the severed rear half of their ship. The Master Chief cryonically freezes himself as he and Cortana wait for rescue while floating toward an unknown planet.

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