After he is betrayed by Arkham, he temporarily allies with Dante near the end, before reverting to his villainous role. Throughout the game, Vergil seeks to undo the seal of his father, Sparda, inside the Temen-ni-gru, and claim the entirety of their father's power for his own, regardless of the effects this will have on the human world. To do so, he needed Dante's half of their mother Eva's amulet, so he lured Dante out with the intent of taking it by force.
Vergil battles Dante three times in the Devil May Cry 3: Dante's Awakening storyline. Their first battle is on the highest level of Temen-Ni-Gru, where Dante is soundly defeated by Vergil, who then takes Dante's amulet. Their second battle is at the very bottom of the tower, where the twins battle to a draw before their battle is interrupted. Their final battle is near the entrance to the demon realm, where Vergil is finally defeated. Should the player achieve certain requirement before the credits finish, the player is shown a cutscene with Vergil rising to his feet in a lake of blood, and looking into the sky to see three large glowing orbs in the sky – Mundus, as he first appeared in Devil May Cry. Vergil decides that if his father was able to fight Mundus, he can too, and charges at the orbs with his sword ready. Though Vergil survives his encounter with Mundus, he becomes enslaved and his name is changed to Nelo Angelo. Dante encounters Nelo Angelo three times in Devil May Cry, and each time Nelo Angelo sees Dante's half of the amulet, he flees the battle. In their final encounter, Nelo Angelo uncovers his face to reveal that he is Vergil. In the end, Nelo Angelo appears to explode, leaving his half of the amulet behind.
Although Vergil himself does not make an appearance in Devil May Cry 4, his sword Yamato does, as a major part of the plot. He is mentioned in passing by Dante, but not by name.
The character is voiced by Daniel Southworth in Devil May Cry 3: Dante's Awakening.
Vergil appears in Ultimate Marvel vs. Capcom 3 as one of the twelve new additions to the game, with Daniel Southworth reprising his role in English and Hiroki Hirata taking up the Japanese voice role. His DLC costume is Corrupt Vergil. He plays very similarly to his DMC3 counterpart, using long ranged normals and specials while dealing a large amount of damage and controlling space with his reach and teleports. His handicaps are his relatively low health and high meter usage.