Eldest begins with Urgals attacking the Varden. This leads to the death of Ajihad, and the disappearance of Murtagh and the Twins. Subsequently, Eragon Shadeslayer, who witnessed Ajihad's death, is summoned to the Council of Elders to help them choose a new leader. They want to choose Nasuada, and use her as a puppet for their wishes. Eragon accepts their choice and agrees to pledge his fealty. However, Eragon stuns the Council by pledging his fealty to Nasuada, not them, and Nasuada is not as easy to control as the Council thought previously.
Meanwhile, Roran has returned to Carvahall and come to the conclusion that Garrow died because of Eragon bringing home the blue stone. He is also trying to tell Sloan that he wants to marry Katrina. They are disrupted, however, when Roran and Baldor, one of Horst's sons, spot the Ra'zac and thirty Imperial soldiers camped nearby. Roran hides in the spine.
Saphira promises Hrothgar to repair the Star Sapphire, Isidar Mithrim. She then gets drunk at a dwarf feast. Then Ajihad's funeral is held, and Nasuada officially becomes the leader of the Varden. Eragon, in deference to Ajihad's last wishes, swears fealty to her. Eragon meets Trianna, a sorceress. She invites Eragon to lead the Du Vrangr Gata, a group of magic users who serve the Varden. Before Eragon can respond, Saphira scares the woman off. Eragon prepares for his departure for Ellesméra. It turns out that Orik and Arya will accompany him. Nasuada's first action as the leader is to move the Varden to Surda, a small, neutral country south of the Empire. Eragon and Saphira say goodbye to Angela and Solembum, who will be accompanying the Varden. The next day, as they are about to leave, Orik announces that Eragon is invited into Dûrgrimst Ingeitum, the clan that Orik and Hrothgar belong to. Eragon accepts, and they leave.
Roran hears from one of Horst's sons, Albriech, that the brewer, Quimby, is dead and that he was eaten by the Ra'zac. Roran and several other men, including Quimby's thirteen-year-old son, Nolfavrell, decide to fight back. They kill some soldiers, but some of their own are killed. They build a wall against the Ra'zac, and there is another battle. More villagers die, including ten-year-old Elmund. Quimby's widow, Birgit, has a vendetta against Roran for being related to Eragon and she feels Roran is the cause of Quimby's death. Roran and Katrina are finally engaged. The Ra'zac say that they will enslave the villagers if they give up Roran, and if they do not give Roran up, the villagers will all be killed.
Eragon, Saphira, Arya, and Orik stop at a dwarf city called Tarnag. Not all the dwarves there are happy about Eragon being part of a clan, particularly one clan, Dûrgrimst Az Sweldn rak Anhûin, which hates all Dragon Riders. Eragon visits a dwarf temple, Celbedeil, where he learns about their religion and six deities. They all decide to leave when the city becomes increasingly unstable. The rest of the journey is fairly uneventful. Eragon learns that dwarves have seven toes on each foot, and sees a primitive dragon-like creature in the Beor Mountains. Arya shows Eragon how to act among elves. They travel by raft and donkey until the company of eleven reaches Ceris, an elven outpost. Two elves, Lifaen and Narí, accompany Eragon, Saphira, Arya, and Orik to Ellesméra. They tell Eragon of King Palancar, who lived in Carvahall and led the humans long ago. As they near an elven city, Eragon and Orik are overcome by elvish singing, driving them into a rage when they are held back by their elven guards.
The Carvahall villagers are fighting over what to do. Roran convinces them to escort the women and children into the Spine. He privately asks Katrina to go, despite the fact that she is an adult and Sloan hates the Spine. As they prepare to leave, Sloan discovers everything and is forced to accept that Roran and Katrina are engaged. Sloan betrays everybody by murdering Byrd, the watchman, allowing the Ra'zac to kidnap Katrina and wound Roran in the process. Nevertheless, Roran decides to leave Carvahall and lead the villagers on an exodus to Surda, a small, independent nation south of the Empire. He does not convince all the villagers, however. A few do not go.
In Ellesméra, Eragon and his friends meet Queen Islanzadí of the elves. It turns out that Arya, who is a hundred years old, is her daughter. He also meets Maud, another werecat, and Blagden, a bird who can talk. Eragon is also introduced to another Dragon Rider, Oromis, the "Togira Ikonoka" who shielded Eragon during the battle under Farthen Dûr, and his three-legged golden dragon, Glaedr. It was they who taught Brom, Morzan, and their dragons. Oromis is weak, and therefore cannot take part in the war against Galbatorix, but has woven countless spells around himself to ensure that he will survive long enough to train the next Rider.
Eragon and Saphira begin their training with Oromis and Glaedr. Eragon finds out that he actually cursed the baby in Farthen Dûr. Arya introduces him to a smith named Rhunön who made all the Riders' swords, including Zar'roc. She has sworn an oath that she will never make another weapon. Arya shows Eragon a tree called the Menoa Tree which was once an elven woman. Eragon recalls that Solembum mentioned it in a prophecy of sorts, telling Eragon if he needs a weapon to "look under the Menoa Tree".
At this point, Nasuada and the Varden are in Aberon, Surda's capital. The Surdan king, Orrin, who is relatively young for a monarch, is a chemist. He is worried that Nasuada is taking over his country. Nasuada tells Trianna to magically create lace to raise money for the Varden. Nasuada meets Elva, the cursed baby, who appears to be about four years old. Instead of being shielded from misfortune, she shields others from misfortune. Orrin vetoes the lace idea.
Back in Ellesméra, Eragon has lessons on debating and logic, history and geography, and magic and sword fighting. He becomes fluent in the Ancient Language. Every day he spars with an elf named Vanir. He learns that Orik is engaged to Hvedra, another dwarf. Eragon learns that the Ra'zac ride on their parents, the Lethrblaka. He realizes that not all Urgals are evil. Saphira also has lessons from Glaedr. Eragon begins to experience strong feelings for Arya, but faces the realization that he cannot join her because of the age gap between them. At the same time, he suffers repeated painful attacks from the scar on his back.
Roran and the villagers arrive at the port city of Narda. They find three barges and convince the captain, Clovis, to take them to Teirm. In Teirm, Roran, Gertrude, Birgit, Nolfavrell, Byrd's son Mandel, and Loring, an elder, enter the city in disguise. Gertrude and Mandel go off in search of Angela, and the others visit Jeod in search of a ship. When Nolfavrell is about to reveal something, Roran interrupts by asking about Angela's shop. Jeod answers, and Nolfavrell asks if that was who Gertrude was looking for. Jeod recognizes Gertrude's name from what Brom said, and tells Roran what happened to Eragon and Brom. They pirate a ship to Surda. When they are pursued by the Empire, they bravely lead their enemies across a whirlpool called the Boar's Eye.
Glaedr teaches Eragon and Saphira about dragons. Then there is a celebration called the Blood-Oath Celebration to honor the first Riders. The last art piece that Eragon saw was of Iduna and Neya with a dragon tattoo. The dragon danced around their bodies, and in a voice of fire, spoke to Eragon: "Our gift to you." The dragons (the tattoo, Glaedr, and Saphira) had given Eragon a gift; they make him into an elf-human hybrid, removing all of his scars. Orik, Arya, and even Vanir are impressed. After the blood-oath, Eragon learns that the elves have no religion. He scries the Varden with magic, and the threat of war with Galbatorix seems imminent. Upon hearing of this, Eragon, Saphira, and Orik immediately leave to go to their aid. They stop at Aberon to find out that the battle will be on the Burning Plains.
Eragon arrives to find the situation poised on the edge of war. The armies of the Varden, mixed with the army of Surda, camp on a plain opposite the vast armies of Galbatorix. Some Urgals, led by Nar Garzhvog, who have been freed from Durza's spell, ask to join the Varden. At first Eragon hates the idea, but Nasuada and Saphira convince him otherwise. The battle begins, and Eragon is able to repel the opposing armies for some time using his new-found powers. The tide of the battle shifts back and forth between both sides. With the appearance of the dwarves, the situation changes to favor the Varden. Roran comes with Jeod and the villagers. The appearance of an unknown Dragon Rider who kills Hrothgar with magic turns the tables once again.
Eragon faces off with the strange Rider, and ultimately unmasks him to reveal Murtagh, who had not been killed, but had been taken by the Twins to Galbatorix, and forced to swear allegiance to the king in the Ancient Language. He and his dragon, Thorn, prove to be more powerful than the weakened Eragon, while Murtagh displays an exemplary skill in magic, using spells that would have killed a normal human. Murtagh decides to have mercy on Eragon and Saphira, however, by twisting a way out of his oaths he took in the Ancient Language. Before he leaves, he claims Zar'roc as his own and uncovers a terrible truth: Eragon was the youngest son of Morzan, and is therefore Murtagh's brother. Murtagh also reveals that Galbatorix is working to save the dragon race and reestablish the Riders; but in order to do this, he must capture Saphira, who is the last female dragon in existence. In the end, Galbatorix's army is routed, thanks to the timely appearance of the villagers of Carvahall. Eragon is reunited with Roran, and they agree to work together to rescue Katrina.