"Everybody have a past, even Dragons. And sometimes the past can come back to haunt them. And when it does, you're gonna need to be there for them."
At night, Berk's animals have been mysteriously dissapearing by falling underground, just then, a creature is seen traveling underground and is making it's way around the village and traveling to Hiccup's homestead. From there, Toothless is having trouble sleeping, aware of the danger lurking beneath, Hiccup just tells him to go back to sleep.
The next day, Stoick and Gobber are among the first to discover a huge hole is created in the middle of the village. When Toothless sees it he suddenly roars in anger, Hiccup tells him to calm down as it's only a hole. They then discover that Bucket, whom Mulch is looking for, is already inside the hole and informs them that inside, is a network of complex tunnels.
While Bucket claims that the tunnels are his happy place, something targets him and throws him out with a massive burst of debris. Stoick asks him if he's alright and asks what happened, Bucket explains in fear, that something huge pushed him out of the hole. Toothless breaches in to confront the creature without telling Hiccup, and searches the underground maze.
Suddenly, the ground trembles and the creature exposes himself, revealing it to be a huge Whispering Death as identified by Fishlegs. The Whispering Death wreaks panic and fear, Hiccup asks Fishlegs for information about the dragon but Snotlout asks how to battle it. Stoick arrives along with Thornado to fend off the dragon, but when it gives the dragon a sonic blast, it has no effect on the dragon as Gobber claims it doesn't have ears.
The Riders and their dragons attempt to thwart the dragon, but Toothless springs in, and furiously tells the dragons to back out. Toothless wants to confront the dragon all to himself, and in the ensuing fight, Toothless is unable to finish the dragon as Toothless is unable to fly to himself and the Whispering Death notices this as an advantage.
Stoick orders Gobber to arm a catapult and fire when the Whispering Death is near Toothless, but Hiccup suggests that he can fix this peacefully, when he tries to mount up to Toothless, he gets pushed aside, not allowing him to join the fight, Hiccup is left confused. The Whispering Death unleashes spines, which one of them hits Toothless leg, but still presses on to fight. Stoick orders Gobber to fire and the Whispering Death is assaulted, it seems to fall back to the ground after being hit by boulders. The Whispering Death tunnels its way to escape.
Hiccup sees Toothless harmed by the spine still stuck on his leg, and he gets it out, but Toothless still carries on to keep watch if the dragon returns, Hiccup and the Riders are left confused of what just happened recently, but one thing they are certain is that the Whispering Death and Toothless are fighting against each other but they have to figure out why.
That night, Hiccup is worried for Toothless as he is fully in self-defense right now, even the footsteps of Stoick first seemed as a threat to him. Stoick asks Toothless' condition, Hiccup responds that he's a bit in good condition, Stoick tells Toothless to not worry as they are confident that the Whispering Death won't return anytime soon, hopefully though. As they prepare to rest, Hiccup tells Toothless to take it easy to mend himself and goes to sleep.
Shortly after, Toothless awakens and checks his Rider if he does not notice him, as he intends to find the Whispering Death and probably end him, Toothless gives one more look to their homestead as he makes his way.
The next morning, Hiccup is stunned to see Toothless gone and soon discovers that he fled in search for a confrontation again for the Whispering Death. Hours later at the Academy, Hiccup assembles the Riders in preparation to search for the Whispering Death, and hopefully find Toothless also. Fishlegs ask that what if they get to the dragon before Toothless does, Hiccup suggests they train it. Hiccup asks Fishlegs for any advantage in the Book of Dragons against the Whispering Death, Fishlegs finds no advantage or weaknesses in the Book except the option to avoid the dragon. Despite that, Hiccup presses on to find the Whispering Death as he fears Toothless' life in danger.
As they explore through the forest, they land near two big holes and Hiccup calls out for Toothless if he's already there, he receives no answer. Suddenly the dragons are now raging uncontrollably, Hiccup tells everyone to quiet, the Twins temporarily makes an annoyance, they feel the earth shaking again. The Riders realize that they came too early to the Whispering Death, and the dragon emerges and identifies his intruders, it then retreats back underground.
It emerges back and attempts to assault the Riders as the dragon attempts to tunnel head towards them, Hiccup confronts the dragon and attempts to train it in hopes that it can leave Toothless alone, by reaching out his hand, when the Whispering Death nears his hand, he backs out and returns underground and Hiccup fails to train it.
Hiccup jumps inside the hole and find the dragon again despite Astrid telling her not to do it. Snotlout jokingly then pushes Fishlegs and he falls inside the hole also, Hiccup thinks Fishlegs came in to support him. Hiccup and Fishlegs follows the Whispering Death lurking around it's maze of tunnel networks in attempt to find any advantage to thwart the dragon. When the dragon springs up in front of them, they hide in one of its tunnels. The Whispering Death tries to find the trespassers, unbeknownst to the dragon Hiccup and Fishlegs are just in it's side.
Fishlegs suddenly points to Hiccup a bite mark in the Whispering Death's body. Hiccup is surprised to find out as Fishlegs explain to him that the bite mark was formed by a Night Fury. Hiccup and Fishlegs discover that Toothless and the Whispering Death have met before in the past and both hold a grudge against each other, Hiccup wonders how long do dragons keep grudges, Fishlegs responds 'to the death..'. Hiccup and Fishlegs decide to escape the tunnel.
However, the Whispering Death spots them and they attempt to flee as fast as possible. When they reach the opening, Hiccup lifts Fishlegs to reach Astrid's hand and make it to the surface. However, Hiccup finds himself trap as he is unable to reach Astrid's hand no matter the effort, the Whispering Death is traveling to him fast. Hiccup has no choice but to brace himself as the Whispering Death charges him with mass dirt and debris causing him to burst out of the hole.
The Whispering Death sticks out it's head to devour Hiccup as they he plummets down towards it's mouth, luckily, Stormfly manages to rescue him in time. The Whispering Death is now in it's aggressive state after Hiccup and Fishlegs trespass inside it's home, when Hiccup attempts to thwart it with dragon nip, the Whispering Death does not buy it and throws it to the dragons, leaving them passed out and the Riders' defenseless. Hiccup is open for ideas, Snotlout recommends that they run for their lives.
The Whispering Death pursues them until Toothless finally makes it's arrival and fends off the Whispering Death and they resume their duel. However, the Whispering Death finds that he is encountered by the other dragons and falls back. Hiccup tries to mount to Toothless again, but Toothless still does not allow his Rider as he brutally pushes him aside, and almost threatens Hiccup. Hiccup tries to talk some sense into him as he requests to only help Toothless, but Toothless refuses and flees. Hiccup tries to follow him to come back, but Toothless threatens him with a warning shot, a message to stay away and he presses on without him.
To Hiccup's dismay, they head home. while flying, Astrid tries to cheer Hiccup by saying that Toothless is only protecting him, but Snotlout denies that as he claims mockingly to Hiccup that Toothless is only determined to fight the Whispering Death alone. Hiccup admits that Snotlout was right, he realizes that Toothless' battle against the Whispering Death is not a fair fight, as he can't fly, so he thinks that Toothless needs him to make the competition fair and they turn back to find him.
Meanwhile, Toothless travels throughout the forest to thwart the Whispering Death to come out and settle their grudge. Overhead, the Riders spot him, Hiccup tells Astrid to get him down near him. Hiccup slowly approaches his battle-hardened attitude dragon to try and disenchant him, and he succeeds. Hiccup finally sees Toothless returning to his old-self, but is short-lived when the Whispering Death emerges and taunts his rival. Hiccup tries to reason with Toothless to choose to back out and go home, it falls on deaf ears as Toothless accepts to settle their rivalry and pushes Hiccup aside as he tries to mount on him.
With the advantage in flight, Toothless is an easy target for the Whispering Death to pick off, as he continuously harms Toothless. Hiccup thinks that Toothless needs their help and the Riders' dragons attempt to support him, but Toothless furiously tells them to back off and leave the fighting to them alone. The dragons respectfully obey his decision.
With no support from the dragons, all the Riders and Hiccup can do is watch their fight. The Whispering Death pushes Toothless to a clearing. The Whispering Death destroys the path to the main ground and Toothless finds himself stuck on a sea stack and becomes an easy target for the Whispering Death. The Whispering Death decides to finish the fight by attempting to push Toothless off the clearing and plummet to his doom.
Suddenly Hiccup takes a step off the cliff and falls, that stuns the Riders and Toothless. Toothless decides to discard the fight and rescue his best friend. With only feet away until they meet their doom, Hiccup manages to mount up onto Toothless and successfully manages set his tail to work, allowing Toothless to fly.
Reunited, Hiccup and Toothless together decide to finish what they started. As they fend off the Whispering Death, Fishlegs notices it getting blind by sunlight, discovering it's weakness, as the dragon can't handle it's sensitive eyes in bright lights. Hiccup and Toothless uses this advantage to get the Whispering Death to exit it's home by blasting it with plasma to it's underground complex, creating a burst of bright plasma erupting in each opening.
The Whispering Death eventually emerges, and Hiccup and Toothless tackles and pins the dragon. In the end, Toothless wins the duel and the Whispering Death is now at the mercy at Toothless. Toothless brutally taunts the dragon preparing to finish him off, but for a moment, has an epiphany that reflects his violent attitude of himself, and decides to spare his long-rival dragon despite his grudge, and the Whispering Death returns home in humiliating defeat.
Snotlout is disappointed that Toothless didn't finish him, Hiccup responds that not all dragon grudges are to the death, Fishlegs decides to change it in the Book of Dragons, the Riders head home.
The next day, Hiccup and Toothless travel to the forest and drop boulders into each hole that was created by the Whispering Death to block passages into it. Their friendship has strengthened as they both promised that they'll always support each other to the enemies that arrives to face them, no matter what.
- Jay Baruchel as Hiccup Horrendous Haddock III
- America Ferrera as Astrid Hofferson
- Christopher Mintz-Plasse as Fishlegs Ingerman
- Julie Marcus and T.J. Miller as Ruffnut and Tuffnut Thorston
- Tom Wilson as Mulch
- Chris Edgerly as Gobber the Belch
- Nolan North as Stoick the Vast
- Zack Pearlman as Snotlout Jorgenson
- Tim Conway as Bucket
- The title is likely a reference to the thriller movie What Lies Beneath.
- The Whispering Death makes it's first appearance in the series.
- This is the first episode to feature a dragon grudge (Toothless fighting the mysterious and deadly Whispering Death with which he has a mysterious and yet unknown reason to have a grudge with. Perhaps these two dragons were once friends until they betrayed each other.)
- According to Fishlegs, the other Berk Dragon Academy dragons didn't aid Toothless in fighting the Whispering Death because they knew it wasn't their battle.
- This is the first time in the series that the inhabitants of Berk use their catapults against a dragon.The first tribe in the series to use catapults against Dragons are the Outcasts.
- One of Snotlout's bullying actions towards Hiccup in this episode, is asking him how it came that Toothless wasn't able to fly on his own. This is a reference to the event in the movie, when Hiccup shot down Toothless with a bola, ripping of a tailfin.
- It appears the Dragon Academy students all carry Dragon Nip (the garlic scented grass that instantly calms and subdues a dragon). This is likely that they do it just in case, if one of the Academy dragons needs to be calmed down immediately.
- The Whispering Death in this episode did not accept the Dragon Nip Hiccup tried to give to it. It sneezed instead.
- When the Whispering Death looks at Astrid and Stormfly in the beginning of the episode, Stormfly's missing the spikes on her head.
- It is shown that the Whispering Death is allergic to Dragon Nip.