Iron Flame is set in the immediate aftermath of Fourth Wing, with Violet Sorrengail recovering at the rebellion headquarters in Aretia. She has just learned that her brother, Brennan, is actually alive, and that her country has been lying to its citizens for hundreds of years to conceal the existence of venin (dangerous dark wielders) who are wreaking havoc just outside Navarre’s protective wards. Navarre’s citizens may be safe from venin, but only at the expense of the Poromish people who live beyond their borders and do not benefit from Navarre’s wards. She has also just learned that the man she loves, Xaden Riorson, is a part of the resistance movement. She is hurt and angry that he kept so many secrets from her and she ends their romantic relationship as a result. 

The Assembly, a group of seven people who make decisions on behalf of the resistance movement, does not initially trust Violet. They do not want to send her back to Basgiath War College with the rest of the cadets who were caught in the attack at Resson, fearing that, as the daughter of General Lilith Sorrengail (the Commander of Basgiath), she will expose their efforts. However, they eventually concede. Before she leaves, Violet learns that Aretia is in danger, as it exists beyond the protection of Navarre’s wards. Violet tells her brother that they should work on reactivating Aretia’s wardstone, but Brennan thinks this is impossible. Instead, he’s focused on procuring a luminary—a device that can create the only type of weapon that can kill venin. 

Violet, Xaden, and the other cadets return to Basgiath, where they lie and claim they were attacked by gryphons in order to explain their absence and the loss of Liam and Soleil. General Aetos cannot prove that they are lying without exposing the truth about venin or the fact that he sentenced them to die, so the group is allowed to graduate. Violet becomes a second-year; Xaden graduates and receives a lieutenant position in the Navarre army, and is sent to the front. Violet finds that she is distressed by Xaden’s imminent departure even though she is not ready to forgive him for keeping secrets. The two are given a weekly leave so that their mated dragons can be together, and they are introduced to Major Burton Varrish, Basgiath’s new Vice Commandment. Violet publicly ends her friendship with Dain, and Andarna enters the Dreamless Sleep while she grows into an adolescent. 

Violet begins to bond with Imogen and the other marked cadets who were part of the Resson attack. At the same time, she distances herself from her other friends—Rhiannon, Ridoc, and Sawyer—because she does not want to implicate them and put them in danger. She also begins to conduct research, with the help of her friend Jesinia from the Scribe Quaderant, on the First Six (the people who created Navarre’s wards in the first place) in an attempt to help Aretia. 

On Conscription Day, Violet is stunned when she recognizes Prince Camlaen Aaric Tauri; he has decided to enter the Rider Quadrant under the fake name Aaric Graycastle. She meets Sloane Mairi, Liam’s younger sister, and tries to protect her, but Sloane resents Violet for her brother’s death and wants nothing to do with her. Violet faces a number of challenges at the start of the school year including an assassination attempt from General Aetos (who is also targeting the other cadets who were at Resson), a top-secret and brutal new class called the Rider Survival Course (RSC), recurring nightmares about the venin Sage, Varrish’s concerning and persistent interest in Andarna, and the return of Jack Barlowe—a student that Violet was thought to have killed the previous year, but who appears to have been miraculously mended. Varrish also starts to target Violet specifically, searching her bags whenever she leaves Basgiath and even ordering Dain to read her memories during an RSC exam. 

Violet and Xaden spend many of their leaves arguing about the nature of trust; Violet insists that their relationship can only work if they tell each other everything, and Xaden maintains that secrets are necessary. During one of Violet’s visits, the pair rekindles their relationship and, in a display of trust, Xaden brings Violet along on a rendezvous with the Poromish gryphon fliers, one of whom is Xaden’s ex Cat Cordella. While Xaden provides them with venin-killing daggers, Violet learns that Viscount Tecarus of the Poromish province of Krovla has the luminary that Aretia so desperately needs. He will give it to them, but only if he can see Violet wield lightning. Violet sees no issue with making such a trade, but Xaden is strictly opposed, fearing that Tecarus will want to add Violet to his “collection.”

Violet returns to Basgiath and finally tells her friends the truth about the venin. They believe her and vow to help with her research. Violet learns that two of the First Six (Warrick and Lyra) kept journals about the creation of Navarre’s wards, and that these journals are kept in the Archives’ sublevel vaults. Violet, Xaden, and other members of Fourth Wing break in and steal them so that they can uncover the secret to fixing Aretia’s wardstone. 

Violet is caught by Varrish, who tortures her for several days to try and get information out of her. However, Violet refuses to break. He brings in Dain and orders him to read Violet’s memories, but Violet shows Dain what really happened in Resson and he stabs Varrish. Xaden then arrives to rescue Violet, finally telling Violet he loves her. Violet finishes off Varrish, after which she, Xaden, and Dain inform the students of Basgiath about the venin. Once the news is out, they bring those who are willing to join the rebellion back to Aretia. A new makeshift war college is set up in Aretia, soon joined by Violet’s sister Mira and a group of riders who have decided to join the resistance as well. 

Andarna finally wakes from her Dreamless Sleep, during which she has grown considerably. Violet is guilt-ridden after learning that the fight at Resson (where Andarna used her powers to save Violet) affected her growth and will likely keep her from bearing a rider. Violet works to translate the texts on the wards but her attempt to fix them is unsuccessful. Angry with her failure, Violet brings her siblings on a secret mission to see Tecarus so that Aretia can at least have a luminary. Tecarus eventually agrees to hand over the luminary if the rebels take the gryphon fliers back to Aretia so they can train with the riders—including Cat. Violet is initially jealous of Cat’s past relationship with Xaden, but Xaden reassures her of his love.
Violet enlists Dain’s help in translating Warrick and Lyra’s journals. The two slowly rekindle their friendship after he apologizes for reading her memories and swearing that he did not know about the venin or intend to get Liam killed. 

During a training mission, Violet, Cat, and Sloane are attacked by Varrish’s dragon, who was likely seeking revenge on Violet for killing Varrish, but Andarna joins the fray and kills him. Violet has an epiphany about the nature of signets and questions Xaden until he admits that he has a second signet—he can read people’s intentions, a form of mind reading that would get him killed if anyone were to find out. Violet is initially upset that Xaden kept another secret from her but the two reconcile after Xaden swears to never keep secrets from her ever again. Violet realizes she has mistranslated a phrase in the journals and seemingly activates the wardstone, but she soon realizes that something is still wrong because the wards are not working at full capacity.

Violet and the rebels learn that the venin army is going to attack Basgiath and they fly over to help. Violet suspects that the venin want to destroy Basgiath’s wardstone, but they arrive too late. Jack, who reveals himself to be one of the venin, destroys the wards. Hundreds of venin descend on the school and everyone goes to battle while Brennan uses his mending abilities to try to fix the wardstone. In the midst of all this, Jesinia finds Violet and tells her that she finally landed on a correct translation, and that a representative of each of the seven dragon breeds is needed to activate the wardstone. Violet is initially stunned—there are only six known dragon breeds—but she eventually realizes that Andarna is from an unknown seventh den. With this new information, she is able to reactivate the wards just in time to stop the venin from taking over Basgiath, but the process kills Violet’s mother who sacrifices herself to power the wardstone. Meanwhile, Xaden fights on the battlefield against the venin Sage who has been plaguing both his and Violet’s dreams. The Sage threatens Violet and, in a desperate attempt to save the woman he loves, Xaden channels magic from the earth and turns venin himself. That night, Xaden goes to Jack’s cell and asks what the cure is, but Jack says that there is none.