On the UEG colony Harvest, there is only peace and prosperity. Watched by two Artificial intelligences, Sif and Mack, the colony produces much of Humanity's food. This peace is interrupted when a Covenant controlled vessel, Minor Transgression, discovers a malfunctioning unmanned human cargo ship. The coordinates registered in the cargo ship's navigation computer lead the aliens to Harvest. A Covenant Unggoy, Deacon Dadab, is alarmed when the ship's Luminary seems to register thousands of Forerunner artifacts and an Oracle (Forerunner A.I.). The opportunistic Kig-Yar plan to take some artifacts for themselves before reporting the discovery to the Hierarchs, and begin surreptitiously raiding human freighters. Unfortunately for the Kig-Yar, the Office of Naval Intelligence had recently organized a strike team to counteract what they believed to be a growing Insurrectionist group, including one Staff Sergeant Avery Junior Johnson. They successfully deceived Minor Transgression into boarding a freighter where they were immediately attacked by Staff Sergeant Johnson and Staff Sergeant Byrne. Staff Sergeant Johnson received a cracked skull from their meeting and Staff Sergeant Byrne was stabbed in the leg with an energy cutlass. This raid marked the first meeting of the humans and Covenant forces, and makes the humans aware of a brand new threat they may be facing. The vessel is self-destructed by its dying captain, with only the Deacon Dadab and his Huragok friend Lighter Than Some escaping in an escape pod.
While the UNSC prepares the Harvest Colonial Militia for a possible alien invasion, two ambitious San 'Shyuum, the Minister of Fortitude and the Vice Minister of Tranquility learn of the large amount of "relics" found on Harvest and begin to plan a coup of the current Hierarchs using this as a fulcrum. To keep the Sangheili from using this discovery as a way to upset the balance of power, they utilize a Jiralhanae-controlled ship, Rapid Conversion, captained by Maccabeus, the Jiralhanae Chieftain at that time, and crewed by his pack of Jiralhanae (including a youthful Tartarus). The two began a secret attempt to seize the planet. This marks the beginning of the powerful alliance between the Jiralhanae and the San 'Shyuum, and the key to their eventual betrayal of the Sangheili leading to the Great Schism later in the war.
Rapid Conversion arrives in the system to find the escape pod containing Dadab and the Huragok, Lighter Than Some, much to the devout Maccabeus' delight. The Jiralhanae use the Deacon as a way to motivate their own lackluster complement of Unggoys and Lighter than Some to repair their intentionally crippled ship. They all soon discover the planet's vast store of reclamations and a message of peace left by Sif and Mack in the form of a crude pictogram displaying a desire for peace. Their Luminary also indicates that there is an Oracle on the planet. The Jiralhanae land two Spirit dropships at a specified date, with only the desire to capture the entire planet at any cost. The attempt at peaceful contact falls apart after an errant Unggoy attacks Harvest Colonial Militiaman Osmo, and the one-sided Battle of Harvest begins.
Meanwhile, the ambitious San 'Shyuum begin their mutiny of sorts by invoking the Prophet of Restraint in a conspiracy that will lead to his removal if revealed. They seek a blessing by the long silent Oracle present on the Forerunner Dreadnought. They visit an old, supposedly senile Philologist, for blessings and advice. When they input the discovery of Harvest and the Luminary's data, the Oracle, which is in fact a fragment of the Forerunner Contender-class A.I. 032 Mendicant Bias, suddenly awakens from eons of dormancy and reveals that they've been misinterpreting their findings. What the Kig-Yar thought were artifacts were actually registering the presence of the Humans on Harvest, which it claims are Reclaimers, and refers to them as his makers. The Minister of Fortitude concludes that these Reclaimers are living Forerunners and were left behind when the rest transcended. Wishing to make amends for his bias, Mendicant begins to power up the Dreadnought to take the humans to the Ark, an act which will destroy High Charity, but is short-circuited by Lekgolo worms exploring the vessel's pathways. Realizing that the discovery of living Forerunners would tear the Covenant apart, the San 'Shyuums swear to secrecy, induct the Philologist into their conspiracy and accelerate their plans for takeover.
On Harvest, the humans begin to resist the assault by the Jiralhanae ship on select towns on the planet by shuttling as many civilians as possible to the planet's capital. Maccabeus is informed that his ship's luminary was broken and he is to destroy the planet, but the devout Chieftain decides to continue his search for relics while attacking the humans. The planet's A.I., Mack, normally responsible for the agricultural JOTUNs, hands over his vast network to his previously concealed doppelganger, Loki, a ship A.I. now implemented as a defense mechanism. The Colonial Militia manages to ferry most of the surviving population to Utgard, the capital, and then begin their plan to send these people to safety aboard the Freighters on top of the seven Space elevators present on Harvest, the Tiara. The Jiralhanae, having stationed their Unggoy forces in the Tiara, unwittingly allow the Huragok Lighter Than Some to come into contact with Loki and the now nearly destroyed A.I, Sif. The Huragok, disgusted by the killing and wishing to end it, shows the A.I. how to duplicate the Forerunner symbol for Oracle and helps lure the Covenant ship in range of the colony's sole mass driver and cripple it. While Johnson leads a small force up the space elevator to clear the Unggoy on board, Tartarus, angered by his uncle's refusal to simply glass the planet, challenges Maccabeus, kills him and takes control of his Pack and counterattacks. During the assault, a jealous group of Yanme'e kills Lighter Than Some. A devastated Dadab slaughters them with his plasma pistol, accidentally irreparably damaging Sif's arrays, and then uses the pistol's last shot to wound Tartarus. Tartarus, who was about to engage Jenkins, loses his energy shields and retreats, but not before obliterating Dadab with the Fist of Rukt. Just after the last human survivors escape the Tiara, Loki fires the mass driver at the Tiara, destroying the station along with Sif and bringing the elevators down on the planet.
The Jiralhanae begin to glass Harvest while the refugees flee. The scheming San 'Shyuum usurp the Hierarchs and become the High Prophets of Truth, Regret and Mercy, and finally declare holy war on the humans, to prevent any of the Covenant from ever discovering their true place as the Forerunner's heirs. The last we hear of Avery is him in the cockpit having sex with Jilan. The newly established High Prophets recommission the Luminary as a means to locate human planets, and thus begins the Human-Covenant war. In the following months, Harvest is glassed while Mack desperately attempts to contact Sif while burying the Tiara's strands with the JOTUNs.