After coming of age, the Avatar is sent by Garon to inspect a Hoshidan fortress above the Bottomless Canyon. However, one of Garon's men, Hans, provokes a battle with the Hoshidans and throws the Avatar's mentor Gunter into the Canyon. The Avatar is found and captured by Hoshidan soldiers, who recognize them as a long-lost member of the Hoshidan royal family. The Avatar is brought to meet their blood relatives and Azura at the capital city. However, soldiers attack the city and a hooded assassin attempts to kill the Avatar. Mikoto shields them at the cost of her life. In the aftermath, the Avatar comes into possession of a legendary sword called Yato, said to belong to the one who will save the world. In the opening battle between the two kingdoms, the Avatar's two families meet, and the Avatar is forced to choose between siding with Hoshido and Nohr. In the Birthright and Conquest routes, the Avatar chooses either their biological or adopted family, respectively. This causes them to be denounced by the other side, and they are gradually forced to fight them.

In the Birthright route, the Avatar helps their Hoshidan kin defend their country from invasion by Nohr. After confrontations with the Avatar, Camilla and Leo's lives are spared. With the help of Elise and Shura, the man who kidnapped Azura from Nohr, the Avatar and their company invade the Nohrian capital. Elise is killed when she attempts to stop the Avatar and Xander from fighting, and Xander falls into despair and forces the Avatar to kill him. The Avatar then faces Garon, killing him with the Yato after it is infused with added power from Ryoma and Takumi's Legendary Weapons. However, Azura dies after having overused her singing powers to weaken Garon. In the epilogue, Ryoma is crowned king of Hoshido and Leo is crowned king of Nohr, and peace is forged between the two kingdoms.

In the Conquest route, the Avatar both fights in the war against Hoshido, and works with their adoptive family to change Nohr's brutal reputation from within. After Azura reveals that King Garon has been replaced by an impostor, the Avatar decides to have Garon sit upon the magical throne of Hoshido, which will remove the false Garon's disguise. During the invasion of Hoshido, the Nohrians spare Hinoka and capture Sakura, while Takumi, whose behavior has become increasingly erratic and violent throughout the war, apparently dies by jumping off of a rampart. Garon orders the Avatar to kill Ryoma. After their fight, Ryoma spares the Avatar the pain of killing their own brother by killing himself. Infusing the Yato with the power of Xander and Leo's Legendary Weapons, the Avatar confronts and kills the false Garon. However, a crazed Takumi suddenly appears and attacks them, and it is revealed he has been long dead and his body is possessed. The Avatar destroys Takumi's body to free his soul. Azura overuses her powers as in the Birthright route, but her death is not seen and she is instead marked as missing. In the epilogue, Hinoka is crowned queen of Hoshido and Xander is crowned king of Nohr, and a peaceful alliance between the two kingdoms is formed.

In the Revelation route, the Avatar rejects both Hoshido and Nohr, and is denounced as a traitor by both. They flee with Azura and one of their retainers through the Bottomless Canyon to the kingdom of Valla. Azura explains that the king of Valla, the dragon Anankos, has plans for humanity's destruction; he is the one who killed and replaced Garon, and he is responsible for Takumi's descent into madness in the Conquest route. Azura also reveals her history as the daughter of the king Anankos usurped, and that a curse placed by Anankos will kill them if they reveal Valla's existence to anyone outside its borders. The two decide to kill Anankos. Fleeing Valla with Gunter, who survived his fall into the chasm, Azura reveals that they must unite the Avatar's twin families before a natural event which will seal the passage for decades.

 

The Avatar travels through Hoshido and Nohr, gradually gaining the trust and allegiance of their hereditary and adopted families. They also learn that their sword Yato is the "Seal of Flames", which when combined with the other families' Legendary Weapons will become the Fire Emblem, capable of killing Ananakos. Once the group enter Valla, the party heads to confront Anankos. During their journey, they battle the resurrected bodies of Mikoto, Azura's mother Arete, and Sumeragi, the latter of whom is revealed to be Mikoto's assassin. During their battle with Mikoto, the Avatar learns that they and Azura are maternal cousins, making the Avatar heir to Valla's throne. The group is eventually betrayed by Gunter, who was possessed by Anankos since first coming to Valla, but the Avatar succeeds in freeing Gunter from Anankos' control. When they face Anankos, they are initially helpless, but Ryoma, Takumi, Xander, and Leo feed the power of their Legendary Weapons into Yato, transforming it into the Fire Emblem. Near death after being defeated, Anankos summons and eats the impostor Garon to regain his strength, but is finally destroyed with the Fire Emblem. In the aftermath, Valla is reestablished on the surface, Azura crowns the Avatar its new ruler, and an everlasting peace is established between the three kingdom

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