Earth and countless other planets were established by families of transhuman and alien royalty for the purpose of harvesting the resulting organisms to produce a youth serum for the elites on other planets. After the death of the matriarch of the House of Abrasax, the most powerful of the alien dynasties, her children, Balem, Kalique and Titus, quarrel over the inheritance, with Balem inheriting an enormous refinery on Jupiter and Titus spending his inheritance on a lavish spaceship. Jupiter Jones narrates that her father, Maximilian, met her mother Aleksa in Saint Petersburg, Russia. After Maximilian is killed in a robbery, Aleksa names their daughter Jupiter, after his favorite planet, and they move to Chicago to live with Aleksa's family.
Years later, Jupiter makes a modest living as a housekeeper to her wealthy neighbors. Wanting to buy a telescope, Jupiter agrees to sell her egg cells, and uses her friend Katharine's name as a pseudonym. At Katharine's house, Jupiter and Katharine are attacked by extraterrestrial "Keepers". Jupiter photographs them, but they erase both of the girls' memories of the incident. Jupiter finds the strange photograph on her phone while waiting at an egg donation clinic, but cannot recall anything about it. During the procedure, the doctors and nurses are revealed to be Keepers sent to kill her, but she is saved by Caine Wise, a former soldier sent by Titus to bring her to him. As Caine and Jupiter flee, their spaceship is destroyed by a squad of Keepers. Caine fends off the attack, kills the Keepers, and hijacks one of their vehicles while protecting Jupiter. Afterwards, Caine realizes that Jupiter must be of great significance to Titus and Balem, who are revealed to have sent the Keepers to Earth to capture her. Caine takes Jupiter to the hideout of Stinger Apini, another former soldier living in exile on Earth. When Jupiter learns that she can control the bees in Stinger's residence, she discovers that she is galactic royalty.
Stinger agrees to help Jupiter. But she is captured by a group of hunters who are supposed to be working for Balem. They have been bribed by Kalique to bring Jupiter to her palace on a distant planet. There, Kalique explains that Jupiter is genetically identical to the dead matriarch, and therefore is the Earth's rightful owner. Supported by Captain Diomika Tsing of the intergalactic police force Aegis, Caine retrieves her from Kalique and takes her to the intergalactic capital planet Ores to claim her inheritance.
In another attempt to lure Jupiter to him, Balem sends Greeghan to kidnap Jupiter's family. On the way back to Earth, Titus's henchmen capture Jupiter and detain Caine, as punishment for not bringing Jupiter to him as promised. Titus reveals to Caine his plan to marry Jupiter, kill her, and claim Earth. Titus then throws Caine into the void of space and attempts to seduce Jupiter, declaring his intention to dismantle the youth serum trade, of which Earth is the next intended source. Caine survives being spaced and returns with Stinger to save Jupiter at the altar before she gets married. Jupiter asks to return home, but learns that her family has been taken hostage by Balem.
At his refinery inside the Great Red Spot, Balem demands Earth in exchange for Jupiter's family. Realizing that Balem cannot "harvest" Earth without her permission, Jupiter refuses. Caine infiltrates the refinery and damages its gravity hull, causing the refinery to begin collapsing. While the occupants evacuate the refinery, Tsing's ship moves in and rescues Jupiter's family. Jupiter survives the collapsing structures, only to land at the feet of Balem, who tries to kill her. But Jupiter fights Balem off and spares him, but not before the structures collapse and Balem falls to his death. Just as Jupiter is about to suffer the same fate, Caine saves her as the refinery is in its final stages of collapse. Tsing opens a portal to Earth and prepares to evacuate, potentially leaving Caine and Jupiter behind. However, she is relieved to find that they have survived and crossed the portal, along with Tsing's ship. Jupiter's family is returned home with no memory of their disappearance, while Jupiter secretly retains ownership of the Earth. Caine's rank in the Legion is restored, and he and Jupiter begin a relationship.
Channing Tatum as Caine Wise
Mila Kunis as Jupiter Jones
Sean Bean as Stinger Apini
Eddie Redmayne as Balem Abrasax
Douglas Booth as Titus Abrasax
Edward Hogg as Chicanery Night
Maria Doyle Kennedy as Aleksa
Tuppence Middleton as Kalique Abrasax
Nikki Amuka-Bird as Diomika Tsing
Vanessa Kirby as Katharine Dunlevy
Jeremy Swift as Vassily Bolotnikov
Christina Cole as Gemma Chatterjee
Doona Bae as Razo
James D'Arcy as Maximilian Jones
Kick Gurry as Vladie
Tim Pigott-Smith as Malidictes
Gugu Mbatha-Raw as Famulus
Rami Malek as Kester Moorhouse
Ramon Tikaram as Phylo Percadium
Demetri Theodorou as Moltka,
Terry Gilliam as Seal and Signet Minister
Samuel Barnett as Intergalactic Advocate Bob
David Ajala as Ibis
Ariyon Bakare as Greeghan
Charlotte Beaumont as Kiza, Stinger's daughter.