Two years have passed since the events in Book II. Baron Harkonnen fumes as he rushes through his private quarters searching for his guard captain. A slave boy whom the baron had been enjoying attempts to kill the baron. The baron surmises that Feyd-Rautha is responsible for planning the assassination. He quickly surmises the identity of the moles within the baron’s guard, and he orders them to be killed immediately. The baron confronts Feyd-Rautha and chides him for the foolish attempt on his life. He tells the teenager that one day, not too far in the future, he will step down and allow Feyd-Rautha to succeed him. The baron also tells Feyd-Rautha that he will assign Thufir Hawat to watch over him, and Feyd-Rautha realizes that Hawat has been playing Feyd-Rautha and the baron against each other. Feyd-Rautha decides to wait, for now, and see what his uncle’s plans are regarding the emperor.

The baron meets with Hawat. Hawat has asked the baron to send a message to Rabban, the baron’s nephew, on Arrakis, but he has not said why. Hawat reveals to the baron his suspicion that the Empire uses the penal colony of Salusa Secundus as a training ground for the Sardaukar. Hawat explains that he believes that the emperor ordered the destruction of the House of Atreides because Duke Leto’s men had trained a small fighting force whose skills nearly match those of the Sardaukar. Hawat points out that Arrakis is as brutal a place for training as Salusa Secundus; the Fremen are an even better fighting force than the Sardaukar. The baron recalls that he once suggested to Count Fenring the possibility of using Arrakis as a prison planet. Hawat suggests that the baron abandon all aid to Rabban and force him to oppress the people even more, so as to make Arrakis into a new Salusa Secundus.

On Arrakis, Paul is preparing to ride a sandworm for the first time. In the last two years, the Fremen have recognized him as a religious prophet. Paul is both a religious and a political leader. He is surrounded by Fedaykin, an elite, highly trained guard. His mother, now the new reverend mother, has become concerned about his role with the Fremen. She has given birth to a daughter, Alia. Chani has also given birth to a child, the product of her unofficial union with Paul. Paul’s son is named Leto, like Paul’s father. The Fremen do not easily accept Alia; since she was still in the womb when her mother took the spice drug, she took in all the memories of the previous Bene Gesserit, so she was aware of herself and was very intelligent even before she was born. Now, barely two years old, she can speak in complete, lucid sentences like an adult and walk easily.

Paul leaves his tent and meets with Stilgar, who gives him a thumper to call the sandworm. Other Fremen give him hooks and poles to use to grab on to the worm’s side. Paul activates the thumper, and soon a giant worm is making its way toward him.

Far in the south of planet Arrakis, Jessica rests in the safety of the sietch warrens. Harah and Alia enter her room. Harah is concerned because Alia has been making the Fremen mothers uneasy. She speaks and carries herself like an adult, and they think she is a witch or possessed by a demon. Harah feels compassion for the young child and says she will try to make the other woman understand.

A Fremen messenger arrives and tells Jessica about a problem: some of the young Fremen men plan to push Paul into challenging Stilgar for leadership of the tribe after Paul rides the sandworm.

Back in the north, Paul succeeds in riding the sandworm he called with his thumper. Stilgar suggests they stop and camp for the night. Both of them realize that the young men will want Paul to challenge Stilgar soon. As they discuss the issue, they spot a smuggler ornithopter flying overhead. Paul decides to teach the smugglers a lesson not to invade Fremen territory.

During the two years between Book II and Book III, Paul establishes himself as a prophet, a powerful religious leader, to the Fremen. His combat skills are now legendary; for example, he has trained a squad of “death commandos” called Fedaykin, the most loyal and deadly soldiers on Arrakis. Alia has also caught the attention of the Fremen. Due to her unique experience in the womb, she is practically a reverend mother, just like Jessica. She is certainly one of the more disturbing creations in science fiction: a two-year-old who talks and thinks like an adult. Jessica accepts the young Alia almost as an equal, allowing her to attend and observe meetings of adults.

One important theme in this section is the idea that oppressive conditions, whether intentionally enforced or not, breed superior humans or, more specifically, superior warriors. The intentionally oppressive conditions of Salusa Secundus and the naturally difficult climate of Arrakis make life on both worlds a miserable experience, but ideal for breeding potent fighters. There is a significant difference between the two worlds: the Sardaukar are bred to fight on any world, whereas the Fremen know only how to fight on Arrakis. A Fremen would be beaten if he were to meet an opponent armed with a body shield. Thus, training and technological development must go hand–in–hand with the oppressive conditions that breed tough individuals.

Paul realizes that the Fremen know only about hardship and killing. The dream that Kynes offered to them, the dream of a lush garden world, was the goal that unified and strengthened the Fremen. A new dream is replacing the dream of turning Arrakis into Eden: the dream of Paul as a savior. Paul recognizes that this dream threatens to sweep far beyond Arrakis and throw the universe into a bloody jihad. The other result of breeding such warriors is that they require some sort of glue, such as a cause to rally around or support, so that they do not give in to despair. On Salusa Secundus, the driving factor is wealth and power; on Arrakis, it is the hope of a world without strife, and after the rise of Paul, it is a dream of a universe of nothing but strife.

The idea of replacement or recycling is also important to the Fremens and Bene Gesserit, particularly as a way of preserving both the ecology of the planet, as well as the history and beliefs of the people. Water is scarce on Arrakis, so the Fremen use the water from the dead corpses to replenish their wells. When Paul kills Jamis, the Fremen remove his water and place most of it in their special wells to transform Arrakis eventually into a lush Eden. The Fremen offer some of the water to Paul, suggesting that Paul is being reborn, or reincarnated, into the Fremen clan. Because Jamis’s water is recycled and shared with the world, his life force is living forever, since his water is providing life to others.

Similarly, the role of the reverend mother lives forever, even if the person in that role does not. Jessica replaces the dying woman as the reverend mother, and as a result, she gains the spirit, or life force, of all the other reverend mothers before her. The history of the Bene Gesserit people is preserved because of the reverend mothers’ ability to pass down their secrets and stories from generation to generation. Even names are recycled in Dune: Paul calls his son Leto after his dead father, Duke Leto. Paul seeks to preserve his father’s name and history, just as the Fremen people seek to preserve their land and their hope of a better future.