The Efrafan Owsla flee the collapsing caverns leaving only Woundwort, Vervain, Moss, and a handful of officers alive. Realizing that not even the cave-in will stop General Woundwort from trying to destroy them, Hazel, Fiver, and Bigwig make preparations to wage war on Efrafa with Pipkin recruiting all of his animal friends. Fiver meanwhile senses that Campion is not dead, and indeed the Efrafan captain manages to pull himself free from the rubble of the caverns alive but horribly scarred. He meets the Black Rabbit of Inlé, who tells him his time has not yet come and that he has a special destiny in store for him. Meanwhile Moss, seeing that Woundwort is going mad, teams up with a doe named Heather to overthrow him but the Watershippers attack Efrafa in full force.

Following the liberation (and destruction of Efrafa), the Efrafans move into Watership Down with Moss, the highest-ranking surviving officer, as their reluctant leader. Tensions are high as three of the other surviving officers try to bully Pipkin and end up getting into a fight with Bigwig. Meanwhile, Woundwort has survived and runs into two other rabbits in a swamp, letting them sink to their deaths in a mire after they refuse to swear loyalty to him. The Black Rabbit of Inlé shows this to Campion and tells him that his destiny is stop Woundwort, who "threatens the world of the living." Campion has a horrible vision of Blackberry in danger, and himself being threatened by a fierce green rabbit. Meanwhile, Moss and Heather decide to take the rest of the Efrafans to start a new warren elsewhere.

The Junior Owsla and Kehaar help an orphaned Hawk survive, whilst at the same time trying to prove to Hazel they are responsible enough to go on solo patrol. What they don't know is that Hazel has been secretly watching them save the Hawk.

Undercover, Woundwort begins to gain the trust of the rabbits at Redstone Warren. He has to fight off his own allies in order to finally gain there trust. Meanwhile, Blackberry finds out about Campion.

Woundwort works his way to chieftainship of Redstone. Meanwhile, Kehaar decides to leave the warren for good with his new mate Gluck.

Woundwort discovers that a human construction crew plans to bulldoze Redstone. He and Vervain travel to the Warren of the Shining Wire where he tells Cowslip he will show him Redstone destroyed if Cowslip will give him his seer, Silverweed. Meanwhile, Hickory and Flax talk of revolt against "Weedstalk" while Marigold races to Watership Down to warn Hazel and the others of Woundwort's return. The wandering Campion stumbles across a new warren, Darkhaven, populated by savage rabbits who await the prophesized return of "the Dark One." He becomes their chief after he defeats their strongest warrior, Granite, winning the respect of a tough doe named Spartina.

Woundwort, Vervain, and Silverweed arrive at Darkhaven just in time to meet up with Campion. At the same time, Hannah learns magic so that she can help her friends.

Silverweed traps Fiver in a twisted dreamworld illusion, allowing him to invade Fiver's mind and see through his eyes to learn the location of Watership Down for his master, Woundwort. Fiver manages to fight off Silverweed's hold, but not before Silverweed deduces that Watership Down is "in the high hills, near a lone beech tree." Hazel realizes how dangerous Silverweed is so he and the others journey to Darkhaven with the intent of kidnapping him. Meanwhile, Campion and Blackberry have the same idea, whilst Granite becomes Woundwort's new second-in-command when he challenges Vervain to single combat. Vervain forfeits rather than face the stronger Granite.

Spartina is sent by Woundwort to befriend Hazel and the others and act as a spy for him. However Silverweed soon learns of her real objective. If Spartina does not return to Darkhaven by the next full moon, she has ordered Granite to kill Blackberry.

Spartina soon gets found out by the other Watership Down rabbits and she confesses everything, even admitting putting Blackberry in danger. After finding out about Spartina's betrayal, Woundwort uses her and Blackberry to make Campion confess where Watership Down is and to lead his army into battle there.

The Watership Down rabbits prepare for the last battle with Woundwort while Blackberry, Spartina and Campion plan their escape from Woundwort.

It's time to end the battle once and for all. Both sides collide and there can be only one winner. Bigwig goes one on one with Woundwort and Hannah plans to use 'the magic' to finally be rid of Woundwort forever. Silverweed knows that a high price must be made to use it so he plans to use it, instead of Hannah.