After the destruction of House Atreides by House Harkonnen, Princess Irulan, daughter of Padishah Emperor Shaddam IV, reflects on her father’s betrayal of the Atreides. On Arrakis, Stilgar’s Fremen escort Paul Atreides and his pregnant Bene Gesserit mother, Lady Jessica, to Sietch Tabr. While some Fremen suspect them of being spies, others, including Stilgar, see signs of the prophecy that a mother and son from the “Outer World” will bring prosperity to Arrakis.
The Fremen accept Paul, but Stilgar informs Jessica that she must succeed the dying Reverend Mother of Sietch Tabr by drinking the Water of Life—a drug fatal for males and untrained women. Using her Bene Gesserit training, Jessica transmutes the liquid, surviving and inheriting the memories of all past Reverend Mothers. The liquid prematurely awakens the mind of her unborn daughter, Alia, enabling Jessica to communicate with her. They agree to focus on convincing the skeptical northern Fremen of the prophecy. Chani and her friend Shishakli suspect the prophecy is fabricated to manipulate the Fremen, but Chani starts to respect Paul when he declares his intention to fight alongside the Fremen, not to rule them.
Paul and Chani fall in love as Paul immerses himself in Fremen culture, learning their language, becoming a Fedaykin fighter, riding a sandworm, and raiding Harkonnen spice operations. Paul adopts the Fremen names “Usul” and “Muad’Dib.” Due to the ongoing spice raids, Baron Vladimir Harkonnen replaces his nephew, Rabban, with his cunning and psychopathic younger nephew, Feyd-Rautha, as the ruler of Arrakis. Lady Margot Fenring, a Bene Gesserit, is sent to evaluate Feyd-Rautha as a potential Kwisatz Haderach and secure his genetic lineage.
Jessica travels south to unite with Fremen fundamentalists who strongly believe in the prophecy. Paul remains in the north, fearing his visions of an apocalyptic holy war will come true if he goes south as a messiah. During a raid on a smuggler spice harvester, Paul reunites with Gurney Halleck, who shows him House Atreides’ hidden atomic warhead stockpile. Feyd-Rautha launches a devastating attack on the northern Fremen, destroying Sietch Tabr, killing Shishakli, and forcing Paul and the survivors to flee south. Upon arrival, Paul drinks the Water of Life and falls into a coma. Though initially angered, Chani is compelled by Jessica to mix her tears with the liquid, which awakens Paul. Now clairvoyant across space and time, Paul envisions an adult Alia on a water-filled Arrakis and a singular path to victory among all possible futures, realizing Jessica is Baron Harkonnen’s daughter.
Paul meets with the southern Fremen war council, galvanizing them by demonstrating his ability to discern their deepest thoughts. Declaring himself the Lisan al Gaib, he sends a challenge to Shaddam, who arrives on Arrakis with Irulan and the Sardaukar. As Shaddam chastises the Harkonnens for their failures, the Fremen launch an offensive, using atomics and sandworms to overpower the Sardaukar. Paul executes the Baron and captures Shaddam and his entourage. Meanwhile, Gurney leads an assault on Arrakeen, intercepting and killing Rabban.
Paul challenges Shaddam for the throne and, to Chani’s dismay, demands to marry Irulan. The Great Houses, summoned by the Baron, arrive in orbit, ready to invade the planet, but Paul threatens to destroy the spice fields with atomic weapons if they intervene. Feyd-Rautha volunteers to be Shaddam’s champion, and Paul kills him in a duel. Irulan agrees to Paul’s request for marriage on the condition that her father lives. Shaddam surrenders, but the Great Houses reject Paul’s ascendancy, so he orders the Fremen to attack the orbiting fleet. As Stilgar leads the Fremen onto the captured Sardaukar ships, Jessica and Alia reflect on the beginning of Paul’s holy war. Chani, refusing to bow to Paul, departs alone on a sandworm.