Vuonna 2552 Madrigal-planeetan ihmiset ovat taistelleet itsenäisyydestään Maasta, mutta kohtalokas kohtaaminen Alien Covenantin kanssa mutkistaa asioita. Master Chief John 117 ja hänen supersotilas "Spartans" liittyvät taisteluun. Taistelun jälkeen Master Chief suuntaa kotiplaneetalleen Reachille Madrigalin eloonjääneiden ja planeetalta löytämänsä salaperäisen esineen kanssa. Mutta kiistanalainen määräys saa Johnin kyseenalaistamaan tehtävänsä ja itsensä. (Owla)

John takes Kwan to an old friend and learns more about the mystery object, which the Covenant and Makee are determined to steal. With the alien threat growing, Dr. Halsey has a plan to deal with John’s unpredictable behavior.

John meets his new partner, and he discovers secrets inside his own memory. Kwan wants to return to Madrigal to continue her people’s fight for independence, but Soren has other plans for her. Makee initiates her plan to retrieve the Madrigal object, with deadly consequences.

Survivors from battle return to Reach. John confronts Dr. Halsey, and the lies of his past. The new prisoner seems to know John better than he knows himself. Determined to understand more, John turns back to the mystery artifact, which shows him something truly startling.

John and Makee come to terms with their shared vision. Halsey has one last chance to save her mission, and herself. As things come to a head, everyone must choose a side.

Beaten, battered, and betrayed, John 117 leads the Spartans on a suicide mission to find the Halo and save humanity. But at what price?

A deadly evacuation mission signals a shift in Master Chief's war with the Covenant. On Reach, a new regime takes the reins at FLEETCOM. John senses a looming threat close to home.

John pushes Silver Team to its limit as he searches for missing Spartans; Kai worries about John's stability. Kwan finds the Rubble is a far more dangerous place in Soren's absence. Halsey seeks the identity of her captor.