The matriarch of the House of Abrasax, a powerful alien dynasty, dies. Her children — Balem (Eddie Redmayne), Kalique (Tuppence Middleton) and Titus (Douglas Booth) — fight over inheritance of her assets.

Jupiter Jones (Mila Kunis) was born on a boat at sea to a Russian mother (Maria Doyle Kennedy). Her father had been killed in a robbery prior to her birth, and her mother named her Jupiter, a name her father had loved. Jupiter and her mother move to Chicago to live with family, where Jupiter grows up.

Years later, Jupiter is working as a maid alongside her mother and aunt. They clean the properties of wealthy citizens of Chicago, scrubbing toilets, and Jupiter finishes each day miserable, whispering to herself about how she hates her life. She dreams of seeing the stars through a telescope she can’t afford to purchase. With the encouragement of her cousin (Kick Gurry), Jupiter decides to sell her eggs to a fertility clinic to get some money and buy the telescope.

At the clinic, the doctors and nurses are revealed as agents of Balem Abrasax sent to kill Jupiter. The assassination is interrupted by Caine Wise (Channing Tatum), a half-human, half-canine former Legion soldier sent by Titus Abrasax to rescue Jupiter. He gets her away from the clinic, but moments before successfully beaming to Titus’ rescue ship, more of Balem’s agents appear and attack. A massive chase scene through Chicago occurs, and Caine and Jupiter finally make it out of the city by car. The two escape and visit Stinger Apini (Sean Bean), a half-human, half-honeybee soldier and former Legion comrade of Caine’s. At Stinger’s house, Jupiter learns Caine and Stinger’s history led to both of them being expelled from the Legion, and Caine was stripped of his wings. Stinger confirms Jupiter is the genetic recurrence of Seraphi Abrasax. The gang is ambushed by hunters sent by Kalique Abrasax, who take them to her palace.

Kalique explains to Jupiter that she is genetically identical to their mother, and the rightful heir to Earth. She demonstrates the restorative properties of RegeneX, the material the family produces. With the help of the Aegis, a type of intergalactic police organization, Caine escorts Jupiter to Ores, the intergalactic capital, to claim her inheritance.

After claiming her inheritance, Titus Abrasax intercepts Jupiter and Caine. He tells Jupiter the manner in which RegeneX is produced, and that the Earth is merely one of many human farms harvestable by Abrasax for its production. He then claims his mother was murdered because she changed her mind about the business and was going to stop production of RegeneX. He convinces Jupiter that with her help, by marrying him, he can continue his mother’s work and bring an end to the harvesting.

Shortly thereafter, Titus reveals his true motives to Caine, which include killing Jupiter after they are married so he can gain authority over Earth. He then throws Caine into space. Caine survives, returns, and rescues Jupiter just before the marriage takes place. They set off to return to Earth.

Before they arrive, Jupiter’s family is taken hostage by Balem and moved to his refinery on the planet Jupiter’s Great Red Spot. Holding the family ransom, he demands Jupiter relinquish ownership of Earth to him, else her family dies. Realizing Balem can’t harvest Earth without her permission, she denies him ownership. Balem retorts by trying to kill Jupiter, only to be rescued by Caine, and the two share a kiss. A battle ensues that leads to Balem’s death, and Jupiter’s family is rescued by Caine and returned home with no memory of the abduction.

Jupiter, having gained a new appreciation for life, returns to her old existence, still the rightful owner of Earth. Caine reveals his wings and status have been restored, and the two fly around Chicago.