The game is a sequel to The Wind Waker, set several months after its events. At the start of the game, Link, Tetra and her pirates are at sea looking for the phantom ship rumored to ply the waters in that area, taking sailors and residents of the nearby islands. Tetra, convinced that the phantom ship is simply a bunch of trouble-making pirates, is determined to teach them that pirates have rules, too. When a mysterious ship appears in the middle of a dense fog, Tetra jumps aboard to explore. As the ship pulls away and begins to vanish with her on board, Link attempts to leap over and save her only to fall into the water himself.
After having a vision of Tetra being surrounded by darkness and calling for his help, Link is washed up on Mercay Island and meets a fairy named Ciela, whose appearance is similar to that of Navi from Ocarina of Time. The fairy has lost her memory and decides to team up with Link. On Mercay Island, Link meets an old man named Oshus who provides him with a sword. Link travels to the far side of the island and rescues Captain Linebeck from the Temple of the Ocean King. In doing so, Link secures the use of Linebeck's customizable steamship to travel throughout the overworld (initially restricted to a single quadrant, but expanded as he acquires more sea maps).
In the first half of the game, Link must rescue three colored fairies: the red Fairy of Power, Reef, from the Fire Temple; the blue Fairy of Wisdom, Nelly, from the Wind Temple; and the yellow Fairy of Courage from the Temple of Courage. However, upon defeating the Courage Temple's keeper, a giant lobster known as Crayk, the rescued fairy is colorless and appears just like Ciela. Ciela wonders why this is, but cannot remember anything due to her amnesia. As Link and Lineback are about to leave Molde Island, Oshus then arrives, using his magical walking stick to fuse Ciela with the colorless fairy to become a yellow fairy, revealing that she is the Fairy of Courage.
Evil Phantom Bellum, the main antagonist, is a plant-like monster that absorbs life-force.Linebeck and Link then set off to pursue the phantom ship. After rescuing four sisters from imprisonment onboard, it is revealed that they are in fact phantoms themselves. Defeating them, Link obtains the key to where Tetra is being held, but he discovers that Tetra has been turned to stone. The old man Oshus then arrives and reveals that he is in fact the Ocean King himself. According to him, a few years ago, an evil plant monster named Bellum appeared, hungry to eat life-force. He used this absorbed force to create powerful monsters, including the dungeon bosses and the phantoms in the Temple of the Ocean King, and used them to seal away the three fairies of Power, Wisdom, and Courage. Ciela, the Fairy of Courage, was able to split herself into two to flee, but in doing so, she also lost her memory. The Ocean King tried to fight Bellum but failed, and he too divided himself into two. Oshus then created the Phantom Hourglass so that someone could use it to venture through the Temple of the Ocean King and defeat Bellum.
Oshus then reveals that the only way to defeat Bellum is by obtaining a weapon known as the Phantom Sword. Oshus asks Link to visit the smithy Zauz on his island. Zauz asks for three steel crystals as necessary ingredients for the sword; the scarlet, azure, and verdure steel crystals are on Goron Island, the Isle of Frost, and the Isle of the Dead, respectively.
Link sails to Goron Island where DaiGoron, the tribe's chief, asks him a quiz to admit him as one of the Gorons. Link defeats Bongorongo in the Goron's Temple and saves MaiGoron, a child Goron that becomes Link's controllable sidekick throughout the temple. Link then sails to the Isle of Frost where he resolves the situation among the snow penguins and snow monkeys. The two races lived peacefully on either side of the island for 100 years, until recently, a snow monkey invaded the snow penguins' village and disguised itself as one of them. Link defeats the Gleeock in the Ice Temple and receives the Azure Steel. Lastly, Link sails off to the Isle of the Dead where he must talk to the spirits of four knights and then finally Mutoh himself, the king of the ancient Daiku kingdom. Link defeats an ancient rock soldier known as Eox and receives the final verdure steel crystal.
After taking the three steel crystals to Zauz and having him forge the Phantom Sword, Link returns to the Temple of the Ocean King and journeys to its lowest floor, where Bellum lurks. Link and Ciela defeat Bellum with the help of Phantom Spheres, which enable Link to freeze time and attack Bellum's weak spot. Bellum then appears to be defeated and Oshus, the Ocean King, then arrives to warp them to safety. Ciela recovers her lost memories. On Linebeck's ship, Tetra is unfrozen and thanks Link for all his trouble. When Link is about to reach out to hold Tetra's hand, Bellum suddenly appears and kidnaps Tetra, then takes over the phantom ship. Link and Linebeck chase after the phantom ship and attack Bellum's tentacles in a marine battle, sinking the ship. Finally, on the ship's ruins, Bellum possesses Linebeck and turns him into a sword-wielding Darknut. Link defeats the possessed Linebeck in a sword fight (as in the style of Ganondorf in Twilight Princess), and Bellum is finally defeated and disintegrates into the Sands of Time.
Oshus reappears as the Ocean King, a blue whale, and says that the Fairies of Power, Wisdom, and Courage must leave with him to their world. Oshus asks Linebeck to make a wish, and Ciela replies for Lineback, saying that he hopes to find treasure. Link and Lineback say their goodbyes to Ciela, with Linebeck pretending to not care about her. Then, the credits roll while a collage of Link's new adventures (in the graphical style of the introduction) is shown. Later, Link and Tetra find themselves aboard the repaired phantom ship. Soon after, Nico sails by and Link and Tetra reboard their own ship. Nico asks what Link and Tetra had been doing for the past ten minutes, and asks Tetra if she just had a bad dream, which Tetra denies. While the pirates argue, Link gasps, noticing that the phantom ship is nowhere to be seen. Link reaches into his tunic and fishes out an empty Phantom Hourglass. Link then runs over to the opposite deck of the ship, where he sees Linebeck's steamboat sailing off into the distance. Link smiles in relief and there, the game ends.