History has it that the leader of the Maori tribe should be the first born grandson of the Paikea, the Whale Rider, but Pai cannot technically inherit leadership; she is a girl, but the last remaining in Paikea's direct line. Her mother died in childbirth, and her twin brother passed away also. Pai's grandfather, Koro, can't help but bond with his granddaughter, but at the same time he is resentful of her existence, blaming her for the upheaval going on in the tribe. He becomes abusive, and Pai decides to move in with her father because of it, but she can't seem to get the ocean out of her blood. She misses the call of the whale and goes home. Her father does not feel a similar call; he moves overseas to Germany to become an artist.
Pai wants to be leader of the tribe one day. She learns the tribe's traditional songs and dances, and its history, but this doesn't impress her grandfather who does not believe a woman can be a leader. Pai knows that this is not true. She knows that she would be a good leader for the tribe, their first female one, and is determined to prove herself.
Koro is a chauvinist, though, and would rather groom a boy to be a leader to whom he is not related than admit his own flesh and blood, a female, could steer the tribe. He leads a cultural school for the village boys, hoping that this will enable him to identify a future leader. Pai follows the lessons without his knowledge, and she also takes lessons from her uncle who won taiaha tournaments when he was her age.
Koro is furious when he learns that Pai is far more suited to leadership than any of the boys he is teaching. She beats star student Hemi, with whom she is friends, at taiaha. To compound his anger, not one of the boys manages to recover the whale tooth that he throws into the ocean, a traditional task that a leader must accomplish. Pai calls out to the whales and one day finds the whale tooth whilst she is swimming. Ancient lore says that this means she is the leader. She realizes that she has to reach out to her grandfather with an olive branch and invites him to her school for a concert of Maori chants, Koro is guest of honor, but runs late for the concert and on his way to the school sees a number of southern right whales beached near Pai's home. The concert is abandoned as the entire community tries to get the whales back into the water, but they are unable to do so. Koro blames Pai for the destruction of the whale pod and tells her not to touch the largest whale because this whale belongs to the Paikea. He will not accept that this is his granddaughter.
Pai waits until her grandfather has turned away then gets onto the back of the largest whale, managing to urge him back into the ocean. The whale leads the pod of beached whales back into the water, and Pai submerges completely. At first the villagers on shore are worried that she has drowned, but eventually she re-emerges and they can see her on the back of the whale going out to see. Her grandmother shows Koro the whale tooth which Pai had found in the ocean. When Pai is rescued from the ocean and taken to the hospital, Koro begs her forgiveness and announces her the tribe's new leader.
Pai's entire family comes together to celebrate her leadership of the tribe and a ceremonial canoe is prepared for her. As it is released into the sea, Pai narrates that she is not a prophet, but that she is the ancestral leader who comes from a long line of chiefs. With a constant movement forwards by the tribe, she knows that they will grow ever stronger.
