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The game begins on High Charity, the mobile capital city of the Covenant. The former Supreme Commander of the Fleet of Particular Justice, Commander Thel 'Vadamee, is being tried before the High Council for his failure to protect Halo. Despite his insistence that the Flood hampered his abilities, the Hierarchs who lead the council, the High Prophets of Truth, Mercy, and Regret, deem him guilty of failing to protect the Sacred Ring. 'Vadamee is then stripped of his rank and branded with the Mark of Shame by Tartarus, the Chieftain of the Brutes.

The story then turns to Earth's Orbital Defense Platform Cairo Station, where Master Chief Petty Officer John-117 receives the new MJOLNIR Mark VI armor from the Master Gunnery Sergeant. Avery Junior Johnson, recently promoted to Sergeant Major, arrives to take John-117 to an awards ceremony overseen by Fleet Admiral Terrence Hood for the dual purposes of awarding meritorious acts and boosting the morale of the surviving human population and noted as a war hero (John-117 has already received all medals except for the "Prisoner of War" medal). The festivities are soon interrupted by Cortana reporting "15 Covenant Capital Ships holding position just outside the kill zone", signaling the start to the Covenant Siege of Earth. UNSC Marine forces along with John-117 protect the station from the invading Covenant Naval infantry but other stations were destroyed by the Covenant. After sending the bomb that the Covenant had placed on the ship back into space (destroying several ships) he landed on the UNSC In Amber Clad and then they head to the surface of Earth to New Mombasa to fight off the Covenant Army, led by the High Prophet of Regret. After the Covenant invasion force is halted by the UNSC defenses, the Prophet of Regret flees Earth with Miranda Keyes, Captain Keyes' daughter, and her detachment in pursuit on the UNSC In Amber Clad. The hasty in-atmosphere jump devastates the city of New Mombasa; destroying the Space elevator and scattering its wreckage for miles around.

The story then turns back to the disgraced Elite Commander, Thel 'Vadamee, who is given the chance of redemption by the High Prophets of Truth and Mercy in taking up the mantle of Arbiter, along with the imminent mortality of the task. The new Arbiter accepts and becomes the will of the Prophets, seeking to complete the impossible task assigned for redemption from his crimes. Thel 'Vadamee is tasked with the assassination of a Heretic Leader, who is disillusioned with the Covenant following the events of Installation 04 up to its destruction. Thel 'Vadamee tracks the Heretic Leader throughout the gas mine (battling the Heretics and the Flood) where the Heretics sought refuge. When Thel 'Vadamee is finally able to face the Heretic Leader, 'Refumee asserts his belief that the Prophets have lied about the Great Journey, punctuating this with the entry of 343 Guilty Spark, whom both Elites consider to be an Oracle of the Forerunners, the ancient race the Covenant hold as gods. Before Thel 'Vadamee could learn more of the claims, the battle resumes, and the Heretic Leader is killed before any meaningful discourse taking place. Tartarus appears to extract him and Guilty Spark, preventing Thel 'Vadamee from learning any information from Spark. He leaves, not knowing what caused the Heretics to betray their sacred oaths to the Covenant.

MC attacks Regret

John-117 battles the Prophet of Regret.

Turning back to John-117's story, Keyes exits slipspace in her ship undetected with the Prophet of Regret unaware that he had been followed. To the surprise of the pursuers, they discover that Regret led them to another Halo Ring. Keyes soon determines that their objective is to Capture the Prophet of Regret and stop the Covenant from firing the Halo Rings; John-117 is dropped onto the surface of Installation 05 with ODSTs to remove Regret. In the course of pursuing Regret, John-117 discovers with the aid of Cortana that the Prophet intends to personally activate Halo, in the belief that it will propel true believers on the Great Journey. Keyes decides that the new revelation about Regret's intentions warrants his death, which John-117 successfully achieves. But before being able to make his escape, the Covenant and High Charity, which has just arrived, attempt to kill John-117 by glassing the area, and he jumps into the lake surrounding Regret's location. Incapacitated from the shock of the Covenant bombardment, John-117 is last seen being dragged into the depths of the lake by the tentacles of the Gravemind, an ancient and highly intelligent Flood form.

The story now shifts back to Thel 'Vadamee on High Charity, in orbit around the ring. The Hierarchs had declared Regret's death to be the Elites' failure, and they were removed as the protectors of the Prophets, who bestow the role to the Brutes, causing more tension between the Brutes and Elites who are already at odds with each other. With the new ring discovered, Truth and Mercy inquire Guilty Spark on how to activate it, and dispatch Thel 'Vadamee to recover the Sacred Icon which will light the ring. Making his way through the Quarantine Zone facing scores of Flood and Sentinels on the surface of Installation 05 seeking the Activation Index, Thel 'Vadamee makes his way into the Library and captures the Index along with Keyes and Johnson after they recovered it from its protective housing. Before he can take possession of the Index, Tartarus again intervenes in Thel 'Vadamee's task. After taking the Index into his own personal possession, Tartarus then reveals that the Hierarchs intended for his death to oust the Elites. His treachery revealed, Tartarus knocks Thel 'Vadamee unconscious down a shaft in the Index chamber to the abyss below.

Beneath the Library, John-117 finds himself in the clutches of the Gravemind, the creature that acts as the sentient intelligence of the Flood. Although Thel 'Vadamee had fallen from a great height, he is saved from plunging to his death by the Gravemind's tentacles. It is within the Gravemind's chamber where Thel 'Vadamee and John-117 meet. In addition, the Prophet of Regret is infected and assimilated into its mass. Also introduced is 2401 Penitent Tangent, Monitor of Installation 05. Both characters act as exposition to Thel 'Vadamee, as Regret remains steadfast to his faith, and the Monitor is fully aware of its status as a weapon. Thel 'Vadamee is further led to question his faith by both John-117 and the Gravemind itself, as they both try to convince the Elite that the Covenant's belief on the Halos is a lie, revealing that the Halos destroy life, not save it. This information, as well the information of the imminent genocide of the Elites lead Thel 'Vadamee reluctantly joining John-117 in the mission to stop the ring from being activated. The Gravemind sends both the John-117 and Thel 'Vadamee to different locations to help stop the Index from reaching its destination. John-117 was sent to High Charity to retrieve the Index while Thel 'Vadamee was sent to the area where the Control Room of Installation 05 to halt the Covenant from activating the rings.

John-117 then enters in the middle of Truth's broadcast. The Prophet, after escaping assassination, flees to the Dreadnought, chased all the way. John witnesses the conflict between the Elites and Brutes, and saves a few Marines along the way. Meanwhile, the Flood, under the control of the Gravemind, crash into High Charity using In Amber Clad. John witnesses Truth's escape on a Phantom, and Mercy infected by the Flood; the Prophet tells the Spartan that Truth is going to Earth to "finish what we started". After boarding the Dreadnought through an energy conduit, he leaves Cortana behind, but promises that he will come back for her.

Meanwhile, Thel 'Vadamee is teleported close to Halo's control room. There, he finds many dead Elites, which were killed by the Brutes. With the help of a few deployed Elites, and sympathetic Grunts and Hunters, he fights his way to meet Rtas 'Vadumee, who is surprised to hear that the Brutes murdered the Councilors. They fight their way to a Scarab, controlled by Sergeant Johnson, who forcefully initiates an uneasy alliance between the humans and the Elites. With the combined efforts of Johnson and 'Vadamee, the Scarab breaches the Control Room doors, and 'Vadamee enters the Control Room to confront Tartarus. In the Control Room, he hears the truth of the Halos directly from 343 Guilty Spark. Still blinded by faith, Tartarus forced Miranda Keyes to activate Halo. Many Zealots and Councilors aid 'Vadamee in his final fight against Tartarus, and eventually managed to kill him. Once Tartarus is defeated, Miranda grabs the Index just in time to stop Halo from firing. However, 343 Guilty Spark says that this has activated a failsafe protocol, causing the Installation to send a signal to the rest of the Halo Array, putting all the Halos on standby for remote activation from the Ark.

The Forerunner Dreadnought arrives at Earth with John-117 on board. He alerts Admiral Hood of his presence, and tells him that he is "finishing this fight".

In a scene after the credits, it appears that High Charity has been completely taken over by the Flood, as thousands of Flood spores are visible throughout the air, floating along the view. The Gravemind speaks of satisfaction of being free of his "empty grave", and suddenly Cortana appears as a hologram on a pedestal in the room. The Gravemind then states that there are questions that linger in his mind, which Cortana must answer. Cortana replies, "Alright...shoot." The screen then turns black before any question is heard.