The prologue of Heir of Ænæria once again visits Sam and Mimir discussing the Enochian threat as well as a new grief that has stricken Ben. The story then rewinds back to Arynn during the battle of Jordysc. Randolph captures her and she then sees Ben get shot in the eye by Longinus and believes him to be dead. Arynn is kept in captivity for weeks until Rhion start killing one another following the power vacuum of King Xander’s death. She is taken to the capital of Vestinia, First Hearth, and begins meeting with Randolph. She trusts him after he reveals he has rescued her childhood friend, Sera, from slavery. Sera and Arynn were in a romantic relationship before she went missing. Arynn agrees to be the legate for Vestinia after Randolph manipulates her into hating the Penteric Alliance.
Back to present day, Ben is in Freztad meeting with Rose and other important villagers to discuss his Nephilim powers and his plans to train with Mimir in the Grand Vault. He goes with Alejandra’s daughter, Mandi, and they become friends. Ben’s training is cut short after Mimir is alerted that another Vault has been opened in Ney, the land of the Orks. He travels with Mandi and Darius along with Sierra and his father’s two robotic raven, Müninn and Hüginn.
Meanwhile, Rose and the leaders of the Penteric Alliance plan for war against Ænæria. It is decided that Rose should be named the Queen of Ænæria and the Penteric Alliance in the hopes of undermining Randolph’s rule in Ænæria. During her time in Freztad she marvels at the vertical farms with the seeds from the Grand Vault. She also becomes friends with Trinity. She reveals to Trinity that she is suffering from nightmares and panic attacks after Julius nearly bled her dry outside the Grand Vault. She is saddened to learn that Kabedge’s husband Vic is dying. He may not survive long enough to see her again after she marches off to war. Kristos is named the new Sentinel Commander and swears revenge against the Ænærians for killing Rakshi. On Rose’s 16th birthday she is officially crowned queen.
Longinus is getting used to her new role as the Legate of Bacchuso. She leads an assault on the young province’s final rebel stronghold. She teams up with the forces of Legate Thatch of Neptuan. After winning the battle she learns that this stronghold actually belonged to the Miners Guild. King Randolph now sees that she is ready to undertake an important mission to a Vault across the Shimmering Sea in a land called Kolpos using the blood from Ben’s eye. The two of them also reflect on the deaths of their loved ones in an attack that destroyed their home village twelve years ago. Ben and his friends traverse the wastelands together, and Mandi reveals that she also lived in same village that was destroyed. Later, they encounter a group of wastelanders and decide that even with Ben’s powers and word, they need to run away or else they’ll be outnumbered and overpowered. Ben still maintains his oath against killing although he starts to wonder if everyone would be better off if he killed Randolph.
Although Rose has experience with leadership, being a queen comes with a new level of responsibility. She is reluctant to send people to their deaths in war. The first phases of battle are planned in Vänalleato. Rose and a small group of soldiers will attack Parvidom because of its strategic importance in southern Ænæria. Meanwhile, a larger force will attack Dark Helm, the capital of Plutonua to capture their weapons factories and interrogate Legate Gatron who mysteriously faked his death and escaped imprisonment in Vänalleato. Rose finds a mysterious letter in her room confirming there is a conspiracy between Vänalleato and Plutonua.
Nico, the captain of the airship heading for Kolpos, attempts to learn more about Longinus. She worries he may suspect that she is a woman in disguise. Not used to making friends, she finds herself oddly pleased by his company. Once they arrive in Kolpos they attack and defeat a village located just outside the Vault which is embedded in a mountain. The new land is named the 15th province of Ænæria and its villagers are enslaved. Longinus opens the Vault and explores it with Nico. They find several siege weapons and staffs that generate lightning. In her excitement, Longinus’s fears are realized and Nico discovers that she is a woman. She makes him swear to secrecy.
Ben and company are surrounded by Orkish scouts and escorted to the Cursed Grove of Tatanka which is located just outside of Ney’s capital city, Kokopolis. Another group of scouts also captured the wastelanders chasing Ben and his friends. Ben attempts to gain entry into Ney with Gal’s fang but it was lost during his initial skirmish with the wastelanders. The scouts state that anyone wishing to enter Ney must pass a trial. They need to survive the Cursed Grove of Tatanka and find the Mouth of Ney. Inside the Cursed Grove, Ben and his friends fight against wastelanders but then have to join forces against ferals—mindless, ghoulish Orks which crave blood and flesh and roam around the Cursed Grove. They eventually defeat the ferals but Ben ends up falling into the Mouth of Ney which is actually a massive waterfall.
Arynn trains with her Rhion and Memnon, her prefect. Combat and leadership do not come easy to her but she decides to use her status as legate to make positive changes. She meets with Estel Crane, the head of Vestinia’s noble family and widow to the late legate Fenwin. They make a deal to end slavery in Vestinia.
Ben wakes up in Kokopolis with serious injuries. A healer named Gus helps Ben with his recovery. Darius starts becoming friends with Liv, one of the wastelanders. Ben, who had been worried about Arynn’s disappearance, learns from Darius and Mandi that she is actually the legate of Vestinia. He becomes angry for keeping this from them. He meets with the leaders of Ney, the Sachems, and also learns that Gus is their ward. Ben learns that he is from Marzora from before Julius formed Ænæria. Ben tells the Sachems about his powers and the Vault in Ney. The Sachems tell Ben that they will ponder his story. During that time Ben amazes Gus with his rapid recovery. Gus helps Ben reunite with Skalle. He tells Ben he knows where the Vault is located. Tired of waiting for the Sachems, Ben reconciles with his friends and tells them about Skalle’s revelation. They team up with group of scouts to go behind the waterfall at the Mouth of Ney—the location of the Vault.
Longinus returns to Bacchuso with the new weapons from Kolpos. She and Nico grow closer and become romantically involved. She also reveals her real name is Sam. Their victory in Kolpos is celebrated with a series of revelations. Randolph proclaims that he wants Sam to be his heir. She announces that the Bacchusan noble, Edwin Dion, will be her prefect. King Randolph also declares he wants to use the new Kolpos weapons to destroy the Grand Vault in Svaldway.
Rose is shot during the battle of Parvidom. Fortunately Shadow, a member of the Miners Guild who resembles the Vänalleatian boy, Felix, with dark skin, blue eyes, and blond hair, keeps her safe. Trinity also helps stabilize her and treats her wounds. The battle is a success and Rose makes her official proclamation to Ænæria that she is their rightful queen.
Arynn leads an assault on Vänalleato with the help of Lady Estel Crane’s riches and Neptuan’s navy. She hopes a victory will earn her the respect of Ænærians and treasures to pay back the Vestinian nobles. Like Rose, she suspects a conspiracy between the town and Legate Gatron. She finds the Grand Elder who reveals he had been buying safety from Plutonua in exchange for a steady supply of slaves. Arynn also learns that the Grand Elder not only sold Sera into slavery, but had attempted to enslave Arynn as well. She kills the Grand Elder and successfully captures Vänalleato.
Ben and the others enter the Ney Vault and discover that there is an Enochian living inside. The Enochian kills nearly everyone—including Skalle, Mandi, and Darius. Liv and Gus are terribly injured. Ben narrowly achieves victory and kills the Enochian with the might of the Voidsweeper. Unfortunately, the weapon is shattered in the process. His robotic bird, Hüginn sends for help and leads the wastelanders to the Vault where they rescue Ben, Gus, and Liv and bring them to a camp outside of Kokopolis where Gus and Liv recover, although they have both lost the use of their legs. It is revealed that Gus is heir of the massacred Marzoran royal family. Ben isolates himself from everyone else for days until finally approaching Gus, announcing that he can heal his legs and that he has finally decided to kill King Randolph.
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