Vergil is the older of the twin sons of Sparda and Eva, and unlike Dante he embraces his demonic heritage and despises his human heritage. His personality is a complete opposite to Dante's; whereas Dante is hot-headed and sarcastic, Vergil is cold blooded and sardonic. He has a lust for power and is willing to disregard anything to obtain the power of his father, Sparda. He uses Yamato, a keepsake from his father, and possesses a sense of style which rivals Dante's.
One year before the events of Devil May Cry 3, Arkham finds Vergil searching for a book in his library, and tells him about the legend of the Temen-ni-gru. Vergil endorses Arkham's plan to raise the Temen-ni-gru, and Arkham reveals that they must undo a number of "seals" as the first step. These seals are in fact fallen angels representing the seven deadly sins, and they must be given their names in order for the seals to be undone. While Arkham researches the location of each seal, Vergil resides in his mansion, along with Alice. However, he wanders through the town at one point, and is confused with Dante by Enzo. The revelation that Dante lives within the city seems to excite Vergil.
As Dante finishes his job to "rescue" Alice, Vergil enters the mansion and questions Rabi about the amulet's power. As Dante and Vergil leave the mansion, they unknowingly cross paths, and Dante is startled after realizing who he passed.
Arkham helps Vergil to break the first seven seals Sparda cast upon the Temen-ni-gru, and then directs him to the Forbidden Land at the base of the tower. Vergil is later seen alongside Arkham at the top of the emerging tower, and when the Hell Vanguard they sent to kill Dante returns, having failed its task, Vergil immediately dispatches it.
Vergil waits at the top of the tower for Dante, and at one point dispatches Arkham to eliminate Lady. When Dante reaches the peak of the tower, the two banter and then ferociously battle. Vergil emerges victorious, and takes Dante's Amulet as his prize. Though Dante's Devil Trigger begins to manifest and Vergil prepares to fight him again, Arkham urges him to ignore Dante, and the two jump off the tower to reenter the Forbidden Land.
As Vergil and Arkham approach the final door to the Sacrificial Chamber, Vergil reveals his knowledge of Arkham's betrayal, and deals him a mortal blow. He then enters the chamber and commences the ritual to open the gate to the demonic world. During this ritual, he is momentarily interrupted by a blinded Beowulf, who has mistaken him for Dante. However, Vergil quickly vivisects the devil, and takes his soul as a Devil Arm.
While Dante was hurrying up to the final seal, Vergil had no luck on unlocking the seal, and was later interrupted by Dante. The twins engaged another fight, which was interrupted by Lady, and the battle ends in a tie. Both demonic brothers are equally wounded, and Jester makes his appearance by announcing that everybody has served their role nicely. Jester later turned back and forth between Arkham and Jester, explaining why Vergil's ritual was incomplete, and why Vergil has failed against Dante and Lady. Arkham completes the ritual, and then plays with the three warriors while waiting for the tower to activate. Once it does, he knocks them off the ascending platform, and Vergil falls into an abyss.
Later, after Dante enters the Netherworld, Vergil is seen passing through the Divine Library, with Lady still huddled up, wounded and in grief, after her battle with Dante. She hears his footsteps and looks up to see who it was, but by that time, he had already gone through the door that Dante took. Vergil later interrupts Dante's fight with the ascended Arkham, and the twins finish Arkham off together. However, Vergil has not given up his goal of obtaining the Force Edge, and the twins are again forced to fight. Though Dante is able to defeat Vergil, he cannot convince him to return to the Human World, and Vergil falls even deeper into the Netherworld.