In the future on a human-populated space colony, Nova Prime, the S’krell extraterrestrial race attempts to take it over with creatures called Ursas, which hunt by “sensing” fear. Ranger Corps, a global peacekeeping organization manages to defeat them with a fear-suppressing technique called “ghosting”, but not before an Ursa kills Senshi, the daughter of their leader Cypher Raige. His son Kitai blames himself for Senshi’s death. He trains to become a Ranger like Cypher but is rejected. Kitai’s mother Faia convinces Cypher to take Kitai on his last voyage before retirement. During flight, their spaceship is caught in an asteroid shower, causing them to crash-land on Earth, which humans had evacuated a thousand years earlier due to an environmental cataclysm.

The two manage to survive, but Cypher’s legs are broken in the process, and the main beacon for firing a distress signal is damaged. Cypher instructs Kitai to locate the tail section of the ship, which broke off on entry to the atmosphere. Inside is the backup beacon, which they can use to signal Nova Prime. Cypher gives Kitai his weaponized cutlass, a wrist communicator and six capsules of a fluid that enhances oxygen intake so he can breathe in Earth’s low-oxygen atmosphere. Cypher warns him to avoid the highly evolved fauna and flora and be careful of violent thermal shifts. Kitai leaves to find the tail section, with Cypher guiding him through the communicator.

Kitai confronts many hazards along the journey; bitten by a paralytic leech after fleeing from a pack of baboon-like monkeys he manages to self-medicate, but damages two of his capsules and does not report to Cypher. After being awakened^{[by whom?]}, Kitai takes shelter just as the thermal shift arrives, where Cypher tells him a story about how he conceived “ghosting” to kill the Ursas.

Kitai reaches a cliffside waterfall and Cypher learns about the broken capsules. Knowing that the only way to continue with two capsules would be to skydive, Cypher orders Kitai to abort the mission, but Kitai, believing that Cypher still sees him as a disappointment, refuses to comply after furiously blaming Cypher’s absence at home for Senshi’s death. Kitai is captured by a large condor and his communicator is damaged. In her nest, Kitai tries and fails to defend her chicks against large panthers before escaping to a river, where he drifts on a raft. After a sleep where he dreams of Senshi, he wakes up to a thermal shift that nearly freezes him to death. The large condor, who had been following him, shelters Kitai at the last moment, sacrificing her life.