Dune Messiah opens on planet Wallach IX where the Guild—comprised of Edric, Scytale, Princess Irulan and the Reverend Mother Gaius Helen Mohiam—discusses their plans to dethrone Paul and put the Bene Gesserit in power. As the Bene Gesserit’s former kwisatz haderach, Paul deeply offended the Bene Gesserit by refusing to bear an heir with Princess Irulan, his political wife, and instead attempting to have children with his Fremen lover, Chani. The Guild establishes that Princess Irulan slips Chani birth control. They make a plan to send a Tleilaxu ghola of Paul’s former sword master, Duncan Idaho—to poison Paul’s psyche and make Paul’s sister Alia attracted to him. The Guild conceals these plans from Paul’s prescience through Edric’s prescience.
The story moves to Paul and Chani’s room on the planet Dune. Paul struggles with a feeling of regret for subjecting Chani to a fate that only he can see coming with his prescience. Meanwhile, Scytale goes to the desert on Dune, kills a man named Farok, assumes his appearance, and kidnaps Otheym’s daughter, a girl who’d been in Farok’s care.
Back in Paul’s city, Paul leads a meeting in which Princess Irulan begs to be allowed to mother the Muad’Dib’s heir. Chani sides with Irulan, pointing out the civil strife that would result from Paul leaving behind no heir. Paul refuses on the grounds that Irulan is too connected to his Bene Gesserit enemies. He wishes that he and Chani could escape to Sietch Tabr, but he knows his name would be left behind to rule in his place.
A few days later, Alia watches through a keyhole as the Guild arrives on Dune, bringing Hayt, the ghola of Duncan Idaho, as a gift. When Paul asks Hayt what his purpose is, Hayt responds that he was sent to destroy Paul. Despite this information, Paul welcomes the Guild to Dune and accepts the ghola, unable to resist its resemblance to Duncan Idaho. Alia feels attracted to Hayt. Meanwhile, the Reverend Mother Gaius Helen Mohiam is imprisoned (Reverend Mothers are banned from Dune). Princess Irulan visits her jail cell, and the Reverend Mother urges Princess Irulan to kill Chani.
A few days later, Alia takes a bath and then practices sword-fighting naked. She is interrupted by Paul and Stilgar, who are upset at what she’s doing. They all have the uncomfortable thought that the Guild may be trying to occasion Paul and Alia to mate. Later, Paul and Edric have a conversation in which Edric accuses the Qizarate of insincerity. After Edric leaves, Paul disagrees with Stilgar and says that his jihad has not brought believers into the light, but rather has resulted in the deaths of 61 billion people.
Alia and Hayt go to the desert to examine a dead body. Alia questions Hayt about his identity. They flirt, and when they get back to the city, Hayt kisses Alia. Alia suspects there is no missing woman and that the body has something to do with a Face Dancer. Later, Paul takes an extra dose of melange and watches the image of the moon falling inside his mind. Despite his power, Paul feels powerless and sees a future without Chani. Hayt appears, and Paul wonders if he is Hayt or Duncan Idaho.
Later, the Reverend Mother Gaius Helen Mohiam sits for trial. Paul, suspecting that the Guild has designs against Chani, offers the Bene Gesserit his sperm if they will spare Chani’s life. Appalled at the idea of artificial breeding, the Reverend Mother refuses. Meanwhile, Scytale tells Edric (whom he despises) to make Hayt destroy Paul faster. Chani is furious when she finds out that Princess Irulan was slipping her birth control, but Paul urges her to forgive Irulan. Chani is upset that Paul duels with Hayt, whom Chani doesn’t trust. When Paul questions Hayt about his identity, Chani realizes that Hayt is more man than ghola. Chani soon becomes pregnant, and the fetus grows alarmingly fast.
Otheym’s daughter Lichna (Scytale in disguise) visits Paul to tell him that Otheym demands Paul visit him on Sietch. Paul can’t find an excuse to not to go. He puts on his stillsuit and goes to Alia’s temple. There, he watches Alia preside over a throng of reverent pilgrims and gets swept up in the mystery and ardor himself. He meets up secretly with his guide, and they depart for sietch. In Otheym’s house, Otheym says that his neighbors are plotting against Paul. He gives Paul Bijaz, a Tleilaxu dwarf who knows the names of Paul’s enemies. As Paul is leaving with Bijaz, a stone burner explodes, burning Otheym’s house and blinding Paul’s eyes.
Despite having lost his eyes, Paul can still see with his prescience. However, many Fremen think that Paul should abandon himself in the desert, as per their rule for blind people. Back in the city, Paul extracts the names of his enemies from Bijaz and puts Korba on trial. Paul charges Korba with aiding enemies in smuggling melange to another planet and in detonating the stone burner. During the trial, Alia makes note of the people in the crowd who were clearly Korba’s accomplices. Meanwhile, Hayt visits Bijaz. Speaking in riddles, Bijaz says that when Chani dies, Hayt will become Duncan Idaho. Bijaz implants Hayt with the order to kill Paul when Paul comes to Hayt in grief. Afterward, Hayt goes to Alia and tells her of the Guild’s plot to mate her and Paul. Hayt then calls medics because Alia has overdosed on melange.
Chani and Paul go to Sietch Tabr. While she is looking out at the desert, Chani goes into labor and is escorted inside. Meanwhile, Paul stands looking out at the desert thinking about how no man can ever rule the universe. Hayt comes up to Paul, and soon after, Paul hears someone scream his name. Paul announces that Chani is dead. Hayt turns to Paul, gripping his knife, but Paul addresses him as Duncan Idaho, and Hayt’s Tleilaxu nature fades away. Suddenly physically and presciently blind, Paul goes to Chani’s body and learns that she gave birth to twins—a boy and a girl—something which Paul had not foreseen. Scytale enters, disguised as Lichna, and offers to revive Chani as a ghola in exchange for control of Paul’s empire. Suddenly able to see through his son Leto’s eyes, Paul kills Scytale. Hayt leads Paul back to his room, where Bijaz again propositions Paul with Chani’s revival. Knowing that the Tleilaxu will condition Chani’s ghola to kill the twins, Paul refuses the tempting offer and orders Hayt to kill Bijaz.
Hayt looks out into the desert and grieves Paul, who has just run into the desert to die. Alia joins Hayt, having just executed all of Paul’s traitors, except Princess Irulan. Hayt comforts Alia over Paul’s suicide, saying that Paul’s act allowed him to escape rule while also obtaining the eternal trust and reverence of the Fremen. Alia and Hat confess their love for each other and go back inside.