Prior to the events of The Taken King, Guardians crippled the Hive invasion force on Earth and the Moon by methodically taking down their field commanders and strategists, including Sardon and Omnigul. The Guardians then banished Crota's soul and eventually killed Crota himself. They also destroyed a Shrine communing with Oryx and killed its protector, Sardok.

Eris Morn alerted Mara Sov of Oryx's arrival, and the Queen set out with the Awoken Armada to Saturn, where the Taken King's Dreadnaught had stopped to refuel. Uldren Sov led his fighter wings to attack the Dreadnaught and engage the fleet of Tombships protecting it, with the Queen and Oryx presiding over the battle from their respective flagships.

With help from her Coven of Techeun Witches, the Queen summoned her Harbingers, deadly orbs that could decimate an army in seconds. The Harbingers bombarded the Dreadnaught, but after the explosions faded away there seemed to be no lasting marks on the battlecruiser. Oryx then fired the ship's superweapon, which ripped a hole through the rings of Saturn and completely destroyed the Awoken fleet. Queen Mara and many other major parts of the Reef's leadership, including Paladin Abra Zire and Techeun Shuro Chi, have since disappeared and are considered MIA, while Petra Venj has advised a remaining Paladin to declare all of them dead.

Attack on Phobos Meanwhile, the Vanguard intercepted a distress signal on all channels, broadcasted from the Skyburners fortress Fleetbase Korus on Phobos. A Guardian is dispatched to Phobos, and they witness a strange new enemy slaughtering the Skyburners. Oryx contacts the Guardians, willing into existence an army of corrupted Cabal and Hive called the Taken. The Guardian defeats these Taken, overcoming Syrok, Word of Oryx. They then attempt to escape the Skyburner Keep via the Aerodrome landing pad, which is riddled with Taken. The Guardian reaches the landing pad and escapes Phobos in their ship.

From then, Oryx's master plan is revealed: He will enslave as many Cabal, Vex, Fallen, and his own Hive as he can, and use them to bring the system into ruin. Initially, one of his consorts, Ecthar (who also fluently speaks English), tells him to only retrieve the strongest of the four races and bring the rest to nigh-extinction, but Oryx objects to Ecthar's advice.

Realizing that the Taken are too deadly a threat to take lightly, the Vanguard send Guardians to rediscover lost powers of their forebearers. The Hunter gains the Nightstalker class and the Shadowshot super ability, the Warlock gains the Stormcaller class and the Stormtrance super ability, and the Titan gains the Sunbreaker class and the Hammer of Sol super ability.