Elder Rider Oromis and his Dragon Glaedr fled to Ellesmera, the capital of the elves' kingdom, while Morzan confronted his old friend Brom, slaying his Dragon. However, Morzan showed mercy to Brom, who later escaped. After the fall of the Riders, Galbatorix reformed the Broddring Kingdom into the Empire, naming himself Emperor. He then focused his efforts into going after the elves and the dwarfs but he was thwarted.

Over the next century, several of the Forsworn were killed either from battle or power struggles, or committed suicide after going mad. Surda declared independence from Galbatorix and became its own country. Brom created the Varden, a rebellion meant to oppose the Empire, killing three of the Forsworn including Morzan; and orchestrated the deaths of five more. Brom and Morzan's wife, Selena, fell in love while Brom was working undercover in Morzan's staff (though this is revealed in the third book). Selena, who already had had Morzan's son, became pregnant with Brom's child. She returned to Carvahall, her brother Garrow's home, to give birth to the child. After begging her brother and his wife to raise her son, Eragon, as their own, she left Carvahall to return to Morzan and her first son. She died soon afterward. When Brom needed to disappear he traveled to Carvahall to live, disguised as a storyteller to be near his son.

The first book in the series started with the attack on Arya, who was carrying a dragon's egg, by Durza, a servant of Galbatorix. Only two other Dragon eggs remain in the citadel in Ilirea, which has been renamed Urû'baen. Arya attempted to send the egg to Brom, but the remaining Eldunarí altered the spell making the egg go to Eragon, because they believed that the egg might hatch for him (revealed in the final book), who finds the egg while on a hunting trip. A few days later, the egg hatches, and Eragon names the hatchling Saphira, becoming a Dragon Rider through their bond. His cousin, Roran, leaves for a job to earn money so he can start a family with his beloved, Katrina. His uncle, Garrow, is killed by King Galbatorix's servants, the Ra'zac, and Eragon flees Carvahall with Brom to hunt down the Ra'zac, unbeknownst to him that Brom is his father. Brom gives Morzan's sword, Zar'roc, to Eragon.

On the journey, Brom teaches Eragon sword fighting, magic, the Ancient Language, and the ways of the Dragon Riders. On the journey they become close friends. Half way through their journey, their camp is ambushed by the Ra'zac and a stranger named Murtagh rescues them, but Brom is gravely injured. In his dying breath, Brom reveals to Eragon that he once was a Dragon Rider and his Dragon was also named Saphira.

Eragon decides to follow his dream of Arya to Gil'ead. Murtagh and Eragon rescue the courier Arya who reveals she is an elf and is in need of the Varden's medical assistance. They flee to the Varden as they are being chased by Urgals to the capital Tronjheim. As they are trapped, Murtagh is revealed to be Morzan's son. The Varden imprisons Murtagh after he refuses to allow his mind to be read, as Murtagh doesn't want them to learn of his parentage. Eragon is introduced to the Varden's leader, Ajihad, his daughter Nasuada, the dwarf King Hrothgar, and his foster son Orik. The Varden are attacked by an army of Urgals. In the ensuing battle, Eragon gets separated from the main fighting and finds himself in a one-on-one duel with Durza. In the duel, Eragon receives a large scar on his back, but Arya and Saphira create a distraction long enough for Eragon to stab Durza through the heart. In the aftermath, Ajihad is killed by a band of Urgals and Murtagh is captured.

In the remainder of the Rider War, Eragon and Saphira learn under the tutelage of Oromis and Glaedr in Ellesmera. During an elvish Blood-Oath Celebration, Eragon is changed by the dragons, giving him elf-like abilities (speed, strength) and healing his back as well as all of his other injuries. Eragon then reveals his true feelings to Arya . After much persistence, Arya angrily rejects Eragon's suit. Meanwhile, Nasuada moves the Varden to the separate country of Surda which is ruled by King Orrin, and Roran moves the villagers of Carvahall to Surda, after their village was destroyed by the Raz'ac, who also captured Katrina. Roran is promoted to Captain while Nasuada allows the Urgals to join the ranks of the Varden. Eragon and Saphira confront Murtagh and Thorn, who slew King Hrothgar. Murtagh bests Eragon, taking his sword Zar'roc, and revealing to him the truth that they are brothers.

Eragon, Saphira, and Roran arrive at Helgrind, where they free Katrina. Eragon and Roran destroy much of Helgrind, slaying the Raz'ac while Saphira kills the Lethrblaka, the Raz'ac's adult form. After which, he goes to the Boer mountains and helps Orik become king of the dwarves. After that, Eragon goes back to the Du Weldenvarden and creates his own sword Brisingr, which bursts into flames each time Eragon speaks its name, and learns that Brom is his real father (he and Murtagh are half brothers) and of the Eldunarí, the hearts of hearts, which is also the source to Galbatorix's power from Oromis and Glaedr.

The Varden captures several cities of the Empire, and Oromis and Glaedr are killed by Murtagh and Thorn, though Glaedr has given his Eldunarí to Eragon and Saphira to further their training. After the defeat of one of the Empire's cities, Nasuada is captured for interrogation by Murtagh, who heals her of her injuries, which causes an identity switch, breaking his oath to Galbatorix. Eragon travels to the Vault of Souls on the ruined Vroengard, which has a massive amount of secret Eldunarí and Dragon eggs hidden from Galbatorix. Taking much of the Eldunarí, he faces Galbatorix and after a fierce battle (after Murtagh and Thorn decide to help them), Galbatorix is slain by Eragon's certain Spell. Meanwhile, Shruikan is killed by Arya.

Murtagh and Thorn retreat to somewhere in the north to have some time to themselves. Nasuada, after a heated debate with the leaders of the Varden, becomes the High Queen of Alagaësia. Arya returns to Du Weldenvarden to help choose a new monarch for the elves after the death of Queen Islanzadí in battle, and is chosen. She takes with her the rescued green dragon egg, which soon hatches for her. Thus, Arya becomes a Rider with her dragon named Fírnen. Near the end of the book, Arya reveals this to Eragon, and Saphira decides to test Fírnen "to see if he has the iron in his bones, and the fire in his belly to match her". They become mates shortly thereafter.

Eragon reworks the magic of the original pact between Riders and dragons to include both Dwarves and Urgals, allowing the dragon eggs to hatch for members of their races. Eragon, coming to the conclusion that there is no safe place to raise the dragons and train new Riders in Alagaësia, begins planning transport of the Eldunarí and the eggs to a region east of Alagaësia, save for two eggs which are kept in Alagaësia: one is to be sent to the dwarves, and the other to the Urgals. Those future Riders will travel to Eragon's new home for training, while new eggs will be sent back to Alagaësia to hatch for new Riders.