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On November 17th, 2552, two weeks after the events of Halo 2, John-117 plummets through Earth's atmosphere using a fragment of the Forerunner 'Dreadnought' he was last seen on in Halo 2. He crashed into an east African jungle, soon after being found by Sergeant Major Avery Junior Johnson on a rescue mission to collect the "Chief". Seargent Johnson, Thel 'Vadam and a handful of Marines, head toward the extraction point. Covenant forces are sighted in the area and Johnson splits the group to reduce their chances of getting spotted. John-117 and Thel 'Vadam continue on their way to the extraction zone with the second squad, fighting off numerous Covenant troops in the process, but upon reaching the extraction zone, Avery Johnson's Pelican group consisting of two Pelicans, are ambushed and shot down by Banshees. Johnson and his men are then captured and taken prisoner by a number of Brutes led by a Brute Chieftain. John-117, Thel 'Vadam, and company fight their way through hordes of Covenant and eventually rescue them, after which a Pelican piloted by "Hocus" arrives and picks them up.

The Pelican brings them to Crow's Nest which is used as a local base of operations by the UNSC. Here, Commander Miranda Keyes and Lord Hood plan a last-ditch effort to stop the Covenant from activating a Forerunner artifact known as the Ark, uncovered outside the ruins of the city of New Mombasa. If activated, this artifact will activate the Halo Array and wipe out all sentient life in the galaxy. Their plan is to have John-117 and a small group of marines punch a hole in Truth's anti-air defenses, so that Lord Hood can initiate a low level air-strike on the artifact. Their planning is quickly interrupted when power is cut and the High Prophet of Truth broadcasts an announcement to all surviving human forces that their doom is inevitable. Soon after that, the Covenant Loyalists discover the facility and mount a heavy assault. After a brief struggle, the outpost is lost and is destroyed by a bomb activated by John-117. Deep underground, John-117 regroups with the surviving Marines and makes his way into the African City of Voi, Kenya via the Tsavo Highway. Sometime afterward, John-117 along with a handful of Marines destroy the Covenant anti-air defenses, Lord Hood leads the last of Earth's military ships against Truth and the artifact. As Hood mounts his attack on Prophet, Truth activates the artifact and creates an enormous slipspace portal, into which all the Covenant ships retreat.

At the same time, a Covenant cruiser controlled by the Flood, a parasitic species which nearly wiped out the Forerunners, arrives suddenly via slipspace and crashes in Voi, the parasite quickly spreads throughout the entire city. As the Human forces attempt to fight the infestation, many are infected by the Flood. The Covenant Separatists lead by Shipmaster Rtas 'Vadum, arrives at Earth and assists the struggle against the infestation. The Elites inform Commander Keyes that a UNSC construct is aboard the crashed Flood ship, and identified it as Cortana. After retrieving Cortana, John-117 returned to the Shadow of Intent to oversee the repairs made by 343 Guilty Spark. However, it is only a recorded message from her. Cortana's message says that the Gravemind is coming to Earth with an army of Flood, and that on the other side of the portal is a solution to the Flood infestation, without having to fire the rings. Lord Hood questions Cortana's plan, assuming that it could be a Flood trap, but John-117 firmly tells Hood that he trusts her.

Lord Hood and his UNSC forces remain on Earth to defend it against the incoming Flood invasion while Commander Keyes, John-117, and the Elites journeys through the Portal. Arriving at the Ark, the Covenant Separatist engages the Covenant Loyalist fleet while the UNSC launches a ground campaign. After landing on the Ark, 343 Guilty Spark helps lead John-117 and UNSC forces to the Ark's Cartographer, the map room of the Ark, to locate the Control Room of the Ark. In order to access the Control Room, the UNSC and the Covenant Separatists must deactivate three shield generators which are inside three separate towers. While SPARTAN-117 and the Arbiter succeed in deactivating the first and second towers, Johnson radios Keyes, telling her that he must retreat due to the heavy enemy assault. When John-117 and the Elites arrived to the third tower, Johnson and his men are nowhere to be seen. After the final shield barrier protecting the Control Room deactivates, the Flood-infested High Charity arrives via slipspace and crashes onto the Ark, releasing many Flood dispersal pods and flood-infested rocks as it falls, causing the Covenant to be even more prone to lighting the rings.

After handling the nearby infestation, John-117 leads the remaining UNSC and surviving Sangheili forces via armored vehicles in an assault on the Citadel containing the Control Room, which is heavily defended by Covenant Loyalist forces. Once inside the Citadel, Truth broadcasts his sermon and reveals the captured Johnson to his followers. Just as Truth is about to force Johnson to activate the rings, Keyes crashes into the Control Room using a Pelican. Knowing she can't kill all of the Brutes, Keyes realizes that she must kill Johnson and herself to stop the rings from being activated. From behind, Truth kills Keyes with a Spiker, and then forcing Johnson's hand on the nearby terminal, activates all of the remaining Halos in the galaxy.

Just as John-117 and Thel 'Vadam reach the top, two Flood Tank Forms confront them. The Gravemind, communicating through the two Flood forms, urges the two to join forces in stopping the initiation of the Halos and Truth. The Flood help John-117 and Thel 'Vadam reach Truth, taking out the Covenant defenses. With the Flood's help, John-117 and Thel 'Vadam slaughtered all the Covenant forces defending Truth. Upon arrival to the Ark's Control Terminal, they find Johnson mourning over the loss of Keyes, and Truth partially infected. Thel 'Vadam, after a short confrontation with Truth over the true purpose of the Halos, executes Truth with his energy sword, claiming he is too dangerous to be kept alive, just as John-117 deactivates all the Halos. Shortly after the deactivation of the Halos, the Gravemind betrays them and prevents the duo from escaping, although Johnson manages to escape using Keyes' crashed Pelican.

John-117 and the Arbiter manage to escape from the Citadel via an access tunnel near the elevator they used earlier. John-117 then experiences a hallucination of Cortana and follows the figure to a control panel. He then activated the panel, surprised to see that the Ark was manufacturing a replacement Halo after the destruction of the previous one. Knowing that the threat of the Flood is undeniably apocalyptic, John-117 decides he will activate the new Halo. Needing an Index in order to fire the ring, SPARTAN-117 journeys into the crashed High Charity to retrieve Cortana, keeping his promise and knowing that she still has the Index she acquired from the original Installation 04. Once retrieved, Cortana instructs the SPARTAN to overload High Charity's engines in order to destroy the Gravemind. Thel 'Vadam arrives via Banshee to assist the SPARTAN in fighting the Flood. The two escape from High Charity before it explodes using a damaged but still flyable Pelican.

The surviving Sangheili and UNSC personnel return to Earth, leaving only Sergeant Johnson, John-117 with Cortana and the Arbiter to make their way to the new Halo. As they make their way to the new Halo's Control Room, Flood forms arrive via Flood Dispersal Pods to prevent the activation of the Halo. From here, they quickly discover that Gravemind is attempting to reconstruct itself on the new Halo. As Sergeant Johnson tries to activate the ring, 343 Guilty Spark fires his defensive laser at him, mortally wounding Johnson, after realizing that it will destroy the installation. The Monitor then turns against John-117 and the Arbiter, blasting the Arbiter out of the Control Room, leaving the SPARTAN to destroy Guilty Spark by himself. John-117 successfully destroys the Monitor with the Spartan Laser and tries to mend Johnson. Mortally wounded, Johnson urged the SPARTAN to send him out "with a bang".

With the Halo activated, John-117 and Thel 'Vadam race towards the frigate Forward Unto Dawn using Johnson's Warthog. With no time to reach the cockpit, John-117 uploads Cortana into the frigate to start taking off before the Arbiter is able to take the controls. The front half of the Dawn, containing the Arbiter, makes it through the portal. However, as Halo shakes itself to pieces during its firing sequence and damages the Ark, the portal deactivates as the other half of the Dawn containing Chief and Cortana enter it. This causes them to rip off from the other half of the ship and be sent to an unknown area of space far enough from the Halo's blast, however, since they didn't come out of the other side of the portal, they never made it back to Earth.

Back on Earth, Lord Hood holds a memorial service in honor for those who died in the Human-Covenant war, with the Arbiter and many Marines in attendance. With Truth dead, the Covenant defeated, and the Flood wiped out, the long and devastating war is finally over. Though he says he can never forgive the Arbiter for what the Covenant did to the human race, Lord Hood sincerely thanks him for standing by John-117 until the end. After the service, the Covenant Separatists returned to their home planet.

After the credits, it is revealed that John-117 and Cortana are still alive aboard the rear section of the Dawn, which had apparently torn off before going through the other side of the portal. The SPARTAN floats to a cryotube and as he climbs in, Cortana comments "I'll miss you." He replies "Wake me, when you need me." If the last level is completed on Legendary difficulty, the section of Forward Unto Dawn that Cortana and John are aboard is seen drifting towards Requiem, the Shield World encountered in Halo 4.