Nine hundred and sixty-six days into its five-year voyage, the USS Enterprise arrives at Starbase Yorktown, a massive "snowglobe"-like station with its own internal atmosphere and cityscape, to replenish dwindling supplies while the crew takes shore leave. Struggling to find continued meaning in their mission, Captain James Kirk has applied for a promotion to Vice Admiral of Yorktown, and plans to name Spock as the new captain of the Enterprise. Meanwhile, Hikaru Sulu reunites with his husband and daughter, Spock and Nyota Uhura have amicably ended their relationship, and Montgomery Scott works to keep the ship operational. Spock also receives word from New Vulcan that Ambassador Spock, his elder counterpart from the original time-line, has passed away.
An escape pod drifts out of a nearby nebula. The survivor, Kalara, claims her ship is stranded on Altamid, a planet in the nebula, and the Enterprise is dispatched on a rescue mission. The rescue turns into an ambush when the Enterprise is overwhelmed by a massive swarm of ships and is badly damaged. The swarm's alien commander, Krall, boards the ship searching for an alien artifact that Kirk had obtained on a recent mission. The swarm rips apart the Enterprise, and the saucer section crashes to the planet as the crew abandons ship in escape pods.
On the planet's surface, Sulu, Uhura and other surviving crew are captured by Krall. Kirk and navigator Pavel Chekov, accompanied by Kalara, find the crashed saucer section. Kalara is discovered to be Krall's ally when she attempts to retrieve the artifact for him. To escape Krall's crew, Kirk activates the still-functional boosters, causing the saucer to lurch forward and crush Kalara. Meanwhile, a seriously wounded Spock and Dr. Leonard McCoy search for the other survivors. Spock tells McCoy of Ambassador Spock's death and that he intends to leave Starfleet to continue his counterpart's work on New Vulcan. Meanwhile, Scotty is rescued by Jaylah, a scavenger who previously escaped Krall's encampment. She takes him to her makeshift home, the wreck of the USS Franklin, an early-generation Starfleet vessel that went missing over a hundred years ago. With Scotty's help, the ship is repaired, and Scotty, Kirk and Chekov, and McCoy and Spock, reunite using the ship as a base. The group plans to raid Krall's camp to rescue the crew and transport them to the Franklin then escape the planet. Meanwhile, Krall coerces a member of Kirk's crew to hand over the artifact that she had kept hidden for Kirk. Krall reveals the artifact is the missing half of an ancient bio-weapon, created by the planet's original inhabitants, that can disintegrate a humanoid life form in seconds. With the device now complete, Krall intends to attack Yorktown and kill its inhabitants, and, using its advanced technology, go on to attack the Federation.
Kirk and the others free the crew as Krall launches from the planet with the bio-weapon, leading his fleet to Yorktown. The Enterprise crew pursues Krall in the Franklin. Scotty transports Spock and McCoy into one of Krall's drone ships where they eject the crew. They discover how the drone vessels coordinate. Krall's communications is disrupted with VHF transmissions, causing mass confusion that results in the fleet's destruction. Krall and his three remaining officers crash in Yorktown. As Krall escapes into the city, Uhura and Kirk discover from the Franklin's logs that Krall is actually Balthazar Edison, the captain of the Franklin. A human soldier from before the Federation's formation, Edison became disillusioned with his life and purpose after peace was established with humanity's enemies. When he and his crew were stranded in the nebula, he believed he had been deliberately cast aside. Having prolonged his life using the planet's alien technology that also physically deformed him, Krall/Edison now plans to destroy the Federation in revenge. Kirk pursues Krall into the Yorktown's ventilation system where Krall attempts to unleash the bio-weapon on the entire station. Kirk forces Krall into a portal, causing the weapon and Krall to be ejected into space, where the weapon consumes Krall. Spock and McCoy save Kirk before he is blown into space.
Kirk is offered the promotion to Vice Admiral, but he opts to remain as a captain. Spock receives a box containing some of the personal effects of Ambassador Spock; reflecting on an included photograph of the aged crew of the Enterprise from the original time-line (circa Star Trek V: The Final Frontier), he chooses to remain in Starfleet and resumes his relationship with Uhura. Jaylah is accepted into Starfleet Academy on Scotty's recommendation. As the crew celebrates Kirk's birthday, they view the construction of their new ship, the USS Enterprise-A.
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