In a prologue, business magnate Peter Weyland speaks with his newly activated android, who chooses the name “David” after looking at a replica of Michelangelo’s statue of David. Weyland tells David that one day they will search for mankind’s creator together. David comments on his unlimited lifespan as compared to his creator’s limited one.
In 2104, 11 years after the Prometheus discovered alien life in the previous film, the colonization-ship Covenant is bound for a remote planet, Origae-6, with two-thousand colonists and over a thousand human embryos aboard. The ship is monitored by Walter, a newer android that physically resembles the earlier David model. A stellar neutrino burst damages the ship, killing some of the colonists. Walter orders the ship’s computer to wake the crew from stasis, but the ship’s captain, Jake Branson, dies when his stasis pod malfunctions, burning him while he’s still asleep. While repairing the ship, the crew picks up a radio transmission from a nearby, unknown planet, dubbed by navigator Ricks as “planet number four”. Against the objections of Daniels (Branson’s widow), the new captain, Oram, decides to investigate.
As the Covenant remains in orbit, an expedition team descends to the earth-like planet’s surface and tracks the transmission’s signal to a crashed alien ship. While on the surface, security-team members Ledward and Hallett divert from the main group to perform field research. Ledward steps away and accidentally steps on alien spores and is soon infected. Meanwhile, Daniels and members of the main group notice cultivated common wheat, but also the complete lack of wildlife or animal sounds. Karine helps the rapidly-sickening Ledward back to the lander where Maggie quarantines them both inside the med-bay. A small, pale, alien creature (neomorph) bursts from Ledward’s back, killing him, and then mauls Karine to death. Maggie attempts to shoot the creature, but accidentally triggers an explosion which kills her and destroys the lander. The neomorph escapes to the planet’s surface while another such creature bursts from Hallett’s throat, killing him.
The neomorphs attack the remaining crew members and kill Ankor. The crew manage to kill one before David, who survived the Prometheus mission, scares away the other and leads the crew to a city full of humanoid (Engineer) corpses. David tells them that upon his and Dr. Elizabeth Shaw’s arrival at the planet, their ship accidentally released a black liquid bio-weapon which killed the native population and that Shaw died when the ship crashed in the ensuing chaos.
After the crew members tell David of their mission, they attempt to radio the Covenant for help, but the surviving neomorph infiltrates the city and finds security-team member Rosenthal alone before decapitating her. David tries to communicate with the creature, but is horrified when Oram kills it. Under Oram’s gunpoint, David reveals that the aliens are a result of his experimenting with the black liquid as a catalyst to create a new species. He leads Oram to an incubation chamber and tricks him into being rendered unconscious by an alien parasite (facehugger). Some time later, another alien creature (xenomorph) erupts from Oram’s chest, killing him.
As the others search for Oram and Rosenthal, Walter, who has found Shaw’s dissected corpse, confronts David after realizing that David had deliberately depopulated the planet when he unleashed the black liquid upon the Engineers. David explains that he believes humans are a dying species and should not be allowed to colonize the galaxy. When Walter disagrees, David disables him and confronts Daniels, telling her he will do to her “exactly what he did” to Shaw. Walter reactivates himself and fights David, allowing Daniels to escape while Lope is attacked by a facehugger. Security member Cole saves Lope, but the now mature xenomorph attacks them and kills Cole. Tennessee arrives in another lander to extract Daniels, Lope, and the victorious Walter. They kill the xenomorph before docking with the Covenant. However, Lope had been implanted with another xenomorph embryo, which bursts from his chest and kills him before escaping into the ship, quickly maturing before killing crew members Ricks and his wife Upworth. Walter helps Tennessee and Daniels lure the creature into the Covenant’s terraforming bay and flush it into space.
The Covenant resumes its trip to Origae-6, and the surviving crew re-enters stasis. Walter helps put Daniels under and she realizes, too late, that he is actually David. A horrified Daniels is unable to escape her stasis pod as she falls asleep while David watches. Now in control of both the ship and its population, David regurgitates two facehugger embryos and places them in cold storage alongside the human embryos before exploring the cargo bay containing the colonists in stasis. He then poses as Walter to record a log explaining that all crew members except Daniels and Tennessee were killed by the neutrino blast at the beginning of the film and that the ship is still on course for Origae-6 before signing off.