The story begins with a focus on the ancient days, when nature and all wildlife were excitedly waiting for the coming of man. Then man arrived from the east, and the relationship between nature and man throve. One relationship in particular -- that between the whale rider and his giant whale -- was exemplary of a symbiotic connection. This whale rider casts spears as life-giving objects to the islands, but one spear he casts 1000 years into the future, which is the time of the story’s young heroine Kahu.
The focus shifts to a herd of whales. The whale mothers look over their young while the single leader whale—the bull whale—reminisces about his own youth so long ago, and the precious time he spent with the whale rider. Now, so many years after their separation, the nostalgia for their time spent together cuts away at the old bull whale. But then the story shifts to Kahu. The narrator of this time period is Rawiri, her uncle. When she is born, her great-grandfather expresses great disdain that she is a girl. He is looking for a suitable successor, which according to local culture ought to be passed from eldest child to eldest child. Porourangi, the girl’s father, is his eldest grandson so he is the successor for that generation. The problem in Koro’s mind, however, is that Porourangi’s eldest child is now Kahu, who—because she is female—is not fit to lead according to Koro.
Thus out of disdain for the girl, Koro refuses to show any love towards her and even refuses to conduct the traditional burial of the birth cord. Instead, Nanny Flowers, Koro’s wife and Kahu’s great-grandmother, must enlist the aid of Rawiri and some friends to help her bury it herself in the town center.
Part I begins by refocusing on the herd of whales. The bull whale leads his herd away from their most-feared predator: mankind. The old whale remembers the days when man and animal were united and in communication, but those are long past. However, he is unable to let go, and thoughts of returning to the place of his youth at whatever cost gnaw at his heart.
Then the story shifts back to Kahu, whose mother dies within a year of Kahu’s birth. Kahu is taken by her mother’s family and raised away from Whangara—the setting of the story, a small town in New Zealand populated by the Maori people. A few years pass in this way. Koro decides to begin a language school to teach the future generations the threatened Maori language, and he also beings culture classes for similar purposes. Kahu returns to Whangara several times when she is able. Each time she comes she expresses love for her family there, but special deep love for Koro her great-grandfather. This love remains unreciprocated, as Koro actively pushes her away. He remains dedicated in his mission to find a suitable successor, and he is doing all he can as leader of the Whangara Maori community to preserve the Maori culture for future generations in a time of spreading modernity.
Part II begins with another short focus on the whale herd. They head towards a sea trench that used to provide them bounty and shelter but they find there an inhospitable and radioactive place. They are forced to travel to other havens as this long-time home for them has become too inhospitable to live in.
Returning to Kahu’s tale, Rawiri narrates that he decided to see a bit of the world when Kahu was in her fourth year. He travels to Sydney, Australia, where he meets several of his cousins and notes that they seem to have drifted away from Maori cultural traditions and have fully embraced the lifestyle of the big city. There, he meets Jeff and the two become fast friends. When Jeff is called back to his parents’ plantation in Papua New Guinea, he asks Rawiri to accompany him and so the two leave Australia for Papua New Guinea. Jeff’s mother and father run a plantation, but his father has become too physically weak to continue with more help, hence their plea to their son to return. Rawiri thus spends two years in that country with Jeff; they attempt to cultivate the land. During the course of his stay, Rawiri has to face racist behavior from Jeff’s social circle, especially his mother. Eventually this racism, combined with Rawiri’s desire to see home again impel him to leave Papua New Guinea and head back to Whangara, New Zealand.
Back home, Rawiri notes that Koro has become even more obsessed in his mission of finding a male successor. The old man feels himself to be under increasing pressure to teach and preserve the cultural knowledge that he and so few others currently possess. As for Kahu, she has returned to stay with her father longer-term. During Rawiri’s absence, Porourangi remarried and his wife had a child: another baby girl. This only upsets Koro more, as he was hoping for a male descendent. Kahu does not mind all this anger from Koro though, and she continues to fervently seek his love and acceptance.
Towards the end of the year, Kahu invites her family to a school ceremony that will include cultural presentations. Rawiri, Porourangi and Nanny all attend, but the seat marked “reserved” next to Nanny—a measure Kahu herself had taken to guarantee a spot for Koro—remains conspicuously empty throughout the ceremony. Kahu herself plays a prominent role in the ceremony. She leads a group of young girls in a traditional dance and also recites a speech she wrote in the Maori tongue. Her speech expresses her utmost desire to please her great-grandfather and to uphold the Maori culture. However, the great tragedy of the event is that Koro never shows up. This brings Kahu to tears.
This part concludes with another momentous event. One day, Koro takes some of his star pupils out to sea. He drops a rock in the sea and once it has sunk to the depths, he tells the boys they must retrieve it as a test of their endurance and strength and ability to lead. Despite their best efforts, they are not able to do so and Koro returns dejected. Back home he cracks under all the pressure and weeps. Later on, Kahu goes out to sea with Nanny and Rawiri, and when they reach the spot above the stone, Kahu dives into the sea and retrieves the stone. She does so by doing what Nanny and Rawiri find extremely amazing: Kahu appears to communicate with dolphins and other sea creatures, and through their aid she is able to retrieve the stone. Nanny orders Rawiri not to tell Koro of this strange incident, as he is not yet ready to accept Kahu’s special status.
Part 3 begins, as usual, by focusing on the whale herd. The bull whale is leading his herd through the frozen waters of Antarctica. A collapsing of the ice there and the life-threatening nature of this collapse forces him to make a snap decision in guiding his herd. He chooses to take them down the paths leading back to the seas of his youth, a decision that causes dismay among the elder mothers because they know his nostalgia for the past is clouding his present judgment. But he leads them on anyway to what they know will be their final journey.
Back in Whangara, big events soon take place. All the whales of a herd come and to the beach and strand themselves there. They will soon die if they are not pushed back to sea. While some humans take advantage of these whales to harvest their meat and organs, most of the locals of Whangara attempt to organize a rescue attempt and deliver the whales back to sea. Rawiri and his biker gang work with the police and rangers to keep whale butchers fro coming near the whales, while the navy is called in to attempt to pull the whales back out to sea. Ultimately, all the dedicated efforts of Rawiri, his friends, Nanny, and all the other locals fail and all of the whales perish on the beach. When Koro returns from a trip he had been on during the ordeal, he remarks with great anguish that this is a sign for them.
The next evening an even bigger event occurs, this time witnessed not by everyone but just by the small Maori community within the town. During the night, Rawiri, Koro, Kahu and Nanny hear a booming sound coming from the sea, as if a great door has just opened, and then they witness a large group of huge whales emerge from the bottom of the sea. At their head is a great bull whale with an ancient sacred Maori tattoo. The bull whale pulls itself onto shore and strands itself there, waiting for its death.
Koro recognizes in this event a spiritual warning to him and his people; their test is to return this ancient whale back to sea because they are so connected to this supernatural whale herd that if it lives they live and f it dies they die. Koro calls a meeting of the local Maori people and impresses upon them the spiritual significance of this event. Their way of life is being put to the test: they can either save the whale or fail and fall into ruin. They organize all available vehicles and manpower down on the beach and attempt all sorts of measures to get the bull whale back to sea, but the giant creature stubbornly resists and continues to wait for itself to die on the shore.
In desperation, Kahu swims out to the whale and climbs up its back after communicating with it. The whale mistakes Kahu for its old master—Kahu’s ancient ancestor, Kahutia Te Rangi. Overjoyed, the whale returns to sea and it descends back into the water with the rest of the herd and Kahu in tow. Kahu agrees to come with the herd in the hopes that she will thus save them and save her own people. She thinks that this will be the last time she will ever see her home and family and that accompanying the herd means losing all that she holds dear, but she sacrifices herself nonetheless and chooses to remain as the whale rider. Back on the shore, Koro finally realizes Kahu’s special status and her suitability to lead. His anguish is now doubled as he must accept that he has been so harsh to the very person he needed so badly this whole time.
The epilogue narrates that the oldest mother whale notices Kahu and realizes that her husband, the bull whale, has mistaken this little girl for her ancestor. She leads to him the conclusion that she is Kahutia’s descendent, and she is the spear he cast into the future and thus she must be returned to her people so she can bring them life-giving benefit and guide them through these troubled times. The bull whale eventually agrees and they return Kahu, now unconscious, to Whangara. When found by humans, Kahu is brought to the hospital to recover and there she is near to Nanny, who collapsed in shock after her dear great-granddaughter left with the whale her Three days have passed since then and Koro and Rawiri have been taking care of the two of them. When Nanny awakens, Koro admits to her that this is entirely his fault, and that he has been stubborn and blind in the matter of Kahu. Later when Kahu also awakens, he tells her for the first time that he loves her. Then the story ends with Kahu telling her dear great-grandfather that she can still hear the singing of the whales.