The city was once ruled by the Matriarch of Avernus, Azimuth, who upon becoming tainted by the corruption of the pillars, began summoning Demons from other dimensions (presumably the Demon Realm ) to attack the city, by the time the fledgling Kain ventured there, the city was in flames and much of the populace had been slaughtered by Demons, who avoided attacking the Cathedral itself, as this was the lair of Azimuth. Once within the Cathedral, Kain was able to find and claim the Soul Reaver blade (and the Wraith armor ) to defeat Azimuth and her demons. Within the walls of the Cathedral he also uncovered the first clues as to the true nature of the corruption of the pillars in the Avernus Catacombs, in the shape of Hash'ak'gik's altar .
In Defiance, Raziel was directed to the city, in search of the Heart of Darkness . Kain; advised of Raziel's progress and shown an image of Raziel overlooking the city in flames; was sent to a time period shortly after his visit in Blood Omen to confront Raziel. They both arrived at the Cathedral, though by the time Kain had arrived, Raziel had uncovered the catacombs, and found out some of its secrets regarding the Hash'akgik cult and Hylden history. Kain and Raziel were to battle in the Cathedral, believing they were enacting the champions' final battle. With Raziel claiming the Heart of Darkness and victory, he left the apparently dead Kain, who had been blasted through a portal to the Demon Dimension and continued his quest to revive Janos Audron . Shortly afterward, Kain managed to escape the Demon Realm and he too left Avernus for the Vampire Citadel . The City was presumably engulfed by the flames and completely destroyed shortly after.
The destruction of Avernus was mentioned in the backstory to Nosgoth with the background of the Lost Seers of Avernus revealing them as descendants of a divinatory order of Cenobites known as the Prophets who had fled Avernus in shock at Azimuth's actions.
- Avernus appears to be named after a volcanic crater in Cumae, Italy; believed to be the entrance to the Underworld in Roman mythology and later known a synonym for the underworld itself.
- There is evidence that some of the other events of the series may take place in Avernus: Mortanius ' punishment of Malek is shown in a darkened room where Malek's body is left a chained skeleton - this closely matches a scene Kain discovers in the catacombs of Avernus; Mortanius' offer to Kain also takes place in an environment that resembles the catacombs.
- The presence of the Earth forge underneath Avernus Cathedral suggests that the Cathedral and possibly the city itself were built on the existing Ancient Vampire ruins.
- The Religion of Avernus is unknown, but much like the rest of Humanity in Nosgoth it appears to have lots of imagery that relates to the Ancient Vampires and may be descended from their worship of the Elder God . Avernus was also the focal point for Nosgoth's alternate religion - the Hash'ak'gik cult and it was likely Cathedral was a front for this darker worship that eventually led to the possession of Mortanius and the corruption of the pillars themselves.
- When surveyed much of the Blood Omen's geography does not exactly match up to the scale shown on maps. Avernus is a special case in that it is very much larger on the inside than the area afforded to it on maps, though this is hardly surprising given that it was Dimension Guardian Azimuth that held sway here.