The Whispering Death first appeared in What Flies Beneath, where it was revealed he and Toothless had a history, and not a nice one. The Whispering Death was a ferocious and merciless fighter, who was determined to kill Toothless. He was also shown to be quite intelligent, being able to figure out Toothless couldn't fly, and thus was an easy opponent. After Toothless defeated him, it is assumed both have moved on and consider the matter closed.
This Whispering Death appeared in episode 14 (What Flies Beneath). He held a grudge against Toothless who had bitten him before Toothless and Hiccup became friends, and got into two fights with Toothless after he arrived on Berk. In the first one, he showed himself to the rest of Berk's dragons, but they all backed off when Toothless attempted to confront the Whispering Death by himself. Hampered by his inability to fly, Toothless wrestled with the Whispering Death until he was shot in the leg by one of the Whispering Death's spikes. In the second fight, Hiccup was prepared to help Toothless, but Toothless refused and tried to manage on his own. Without Hiccup, Toothless was unable to fly properly, so the Whispering Death knocked him out of the sky and used his fire to send him onto a ledge where the Whispering Death attempted to send Toothless into a canyon, which would kill him. Only by accepting Hiccup's help was Toothless able to defeat the Whispering Death, Hiccup deliberately forcing Toothless to accept his aid by jumping off the canyon himself, leaving Toothless to save Hiccup and accept his aid or let his friend die to save his vendetta. After he and Hiccup were able to down the Whispering Death using its weakness to direct sunlight, Hiccup convinced Toothless to spare his foe, which then fled back to its tunnel.
- It has never been revealed how, where and why Toothless and Whispering Death developed a grudge for one another in the first place. However, Rise of Berk hinted that the story may be revealed in a later season.