In the Merethic Era when dragons ruled Tamriel, Durnehviir took part in many battles against other dragons for control of the skies. Instead of fighting, he delved into "alok-dilon", or necromancy. Like many great necromancers, he contacted the Ideal Masters in an attempt to gain their favor. They granted him the power to summon armies of undead from the Soul Cairn, but in return he had to guard a vampire named Valerica who had been trapped in the Soul Cairn by the Ideal Masters. The Masters neglected to inform Durnehviir of Valerica's immortality, and essentially tricked him into eternal servitude. In time, his body became accustomed to the Soul Cairn, making it impossible for him to ever permanently return to Tamriel.
In 4E 201, the Last Dragonborn and Serana journeyed to the Soul Cairn in search of Valerica. Their actions awoke Durnehviir, who attacked the intruders. He was killed by the Dragonborn, but his soul was not devoured thanks to the Ideal Masters' protection. He promptly rematerialized, and hailed the Dragonborn as his "Qahnaarin", or Vanquisher. Humbled by his defeat, Durnehviir allied himself with the Dragonborn. He asked the Dragonborn to use the thu'um to summon him to Tamriel, allowing him to briefly be free of the Soul Cairn. In return for granting his wish, Durnehviir fought for the Dragonborn and passed on the knowledge of a necromantic Dragon Shout. Although Durnehviir's debt to the Ideal Masters had been paid, he remained eternally trapped in the Soul Cairn.
- For game-specific information, see the Skyrim article.