Werthrent was a fire snake from another realm worshiped as a deity by the Serepentians. His heart contains the second Dimensional Key.
At some point in the past, Werthrent connected from its realm of origin with the planet Serepentis, where its inhabitants took it as a deity. Regularly, Serepentians are offered to Werthrent as sacrifices. Since it is believed by The Serepentians that those sacrificed would receive an eternity of joy, many Serepentians willingly volunteer for this. In reality however, those sacrificed end up in a pocket dimension inside Werthrant, where they are kept in an undead state as zombie slaves, suffering for eternity as their minds are being drained by the wicked god.
Years before the events of the series, Ash Graven and her sister Harp were sacrificed to Werthrent by their parents. Harp was the first to go, and seeing her sister get devoured awoke Ash' powers. In her panic, she accidentally killed her parents and several cult members.
In "The Grand Surrender", the Crimson Light's crew realizes that the second Dimensional Key is at Ash's homeworld after H.U.E. took note of her tattoo. Despite feeling intimidated by the thought of returning to Serepentis, Ash relents upon realizing that she could get her sister back. Ash confronts Werthrent and demands that he free her sister. Werthrent instead eats her and the rest of the Team Squad.
Once in the pocket dimension, the team learns the truth about Werthrent's victims. They find the Dimensional Key, which is located in the serpent god's heart. The team is made to solve three riddles from the guardian of Werthrent's heart, Septim. KVN gets rid of Septim by first correctly answering two of his riddles, and then killing him with a Forever Ball. With the guard gone, Little Cato removes the key from the heart, which kills Werthrent and causes the pocket dimension to collapse. Before they escape, Ash reunites with her sister, only to realize that she has long lost her mind, becoming a mindless zombie enslaved to Werthrent. Acknowledging that her sister was long gone, Ash escapes the pocket dimension with Little Cato, and Werthrent is killed. After his death, the ring around Serepentis vanished, suggesting it was part of Werthrents body.
- His name is often misspelled as "Worthred", "Worthrent", and "Worthrunt". The official subtitles for "The Grand Surrender" confirm his name is meant to be spelled as "Werthrent".