Taking place during the Covenant attack on Earth. In the year 2531, the classified UEG colony of Onyx had been designated the headquarters and training ground for the SPARTAN-III Program. However, the UNSC had no idea that the planet was in fact a huge Forerunner construct, integral to the Halo Array, and containing trillions of Sentinels. After John-117's destruction of Alpha Halo, the Sentinels were roused by the disruption of the Halo network and the portal leading into the Shield World at the planet's core began to close. At this time, a small group of Spartan-IIIs were training in a top honors exercise on the surface. After the humans failed to exchange the proper counter-responses, the Sentinels relabeled the "Reclaimers" as aboriginal subspecies and began to exterminate them. Led by Kurt-051, the Spartan-IIIs fought a guerrilla war against the Sentinels until Doctor Catherine Halsey arrived on Onyx and explained the wider situation. Knowing that the Forerunner technology buried in Onyx's core could turn the tide of the war for humanity, Halsey used Forerunner technology to send a message to Fleet Admiral Sir Terrence Hood, requesting reinforcements. Hood deployed Blue Team to Onyx, who stole a Covenant destroyer to reach the planet in time.
Meanwhile, the Covenant Separatists under the leadership of Imperial Admiral Xytan 'Jar Wattinree had deployed a fleet to Onyx to claim the "sacred relics" for their fight against the Jiralhanae and the other Loyalists. Xytan would not live to hear of the results of this mission, as he and the majority of his fleet were annihilated by a UNSC Nova bomb recovered from Reach. After Blue Team made landfall, Fleet Master Voro Nar 'Mantakree's fleet arrived at Onyx, destroying hundreds of orbiting Sentinels before engaging UNSC forces in the Forerunner city below. 'Mantakree personally led the Covenant forces on the surface, before the UNSC Battlegroup Stalingrad arrived and used indirect help from the Sentinels to destroy the majority of the Separatist fleet before being wiped out by reinforcements from Joyous Exultation, with only one ship escaping.
On the surface, the Spartans had discovered the Core Room Antechamber and were preparing to enter the Shield World. They managed to hold off hundreds of Covenant troops before being forced to retreat into the Core, while Kurt-051 sacrificed himself by detonating a couple of FENRIS Nuclear Warheads, killing the entire Separatist force. Following the Core being sealed, Onyx broke up into trillions of Sentinels, guarding the construct. With the Covenant Separatists dangerously depleted, the warlike Sangheili were finally forced to ally with their hated enemy, humanity.