Midna returns Link to the World of Light. She tells Link that he cannot revert to his Human form yet, and that he needs her cooperation to save his friends. In his Wolf form, Link returns to Ordon Village to find it infested with Bulblins.
He acquires the Sword intended for the Royal Family, along with a Shield from the Village. Before Link returns to the wall of Twilight, he is summoned by Ordona, the Spirit of Ordon Spring and one of the four Spirits of Light who preside over Hyrule. Ordona explains to Link that its fellow Light Spirits were slain and robbed of their light by Shadow Beasts, turning Hyrule into a Twilight-covered netherworld. Ordona tells Link that he must restore the light to Hyrule to regain his original form and abolish the Twilight from the land.
Link returns to the Twilight-covered Faron Woods and finds Faron, another one of the four Light Spirits. Faron tells Link that he must recover its Tears of Light from the Insects of Darkness that stole them to rid the Woods of the Twilight. Link does so, and is restored to his Human form. Link finds himself wearing the Hero's Clothes, the same tunic that belonged to the chosen hero of the gods in years past.
Faron tells Link that his transformation into a Wolf was a sign that he is the chosen hero of the gods. He explains that a dark power lies in the Forest Temple deep in Faron Woods, and that Link must obtain it to match the power of the King of Shadows. Link makes his way through the Forest Temple, defeats the monstrous Diababa, and acquires the dark power Faron spoke of, the Fused Shadow. Midna tells Link that there are two other Fused Shadows in Hyrule, and urges him to find them.
Link travels east to Eldin Province, which has been smothered in Twilight. He ventures to Kakariko Village, where he finds the Light Spirit, Eldin. Once again, Link must collect the Tears of Light around the Village to restore the light to Eldin Province. He does so, and reunites with the children of Ordon Village, who had been taken to Kakariko. Link also meets the Village Shaman, Renado, who tells him that they are having trouble with the Gorons of Death Mountain. For some reason, the Gorons have become hostile towards the humans and refuse to grant them entry into their Mines. Renado mentions that Mayor Bo, the Mayor of Ordon Village and Ilia's father, should know how to best the Gorons.
Suddenly, Epona rushes into the Village, but she has become wild and nearly tramples Link. Link manages to calm her, and rides Epona back to Ordon Village to meet with Bo. Bo reveals that he earned the Gorons' trust by defeating them in a Sumo Wrestlin' match using his Iron Boots, which he gives to Link.
Link returns to Kakariko Village, only to find that Colin has been kidnapped by the Bulblins' leader, King Bulblin. Link and Epona chase the monster and his minions into Hyrule Field, where a horseback battle ensues. The chase continues onto the Bridge of Eldin, and Link knocks King Bulblin off the Bridge and rescues Colin. The hero scales Death Mountain and bests the Goron elder, Gor Coron, in a Sumo match using his Iron Boots. The elder proceeds to tell him that the Goron patriarch, Darbus, has fallen victim to the dark power of another Fused Shadow. It turned him into a monster, and the elders were forced to seal him inside the mountain.
He requests that Link enter the Goron Mines and aid Darbus. Link ventures deep into the Mines and finds Darbus, who has transformed into a monster engulfed in flames. Link defeats him and acquires the Fused Shadow that possessed him. After this, Midna tells Link that the King of Twilight's name is Zant, and declares that she opposes his power. The relationship between the Gorons and humans of Kakariko Village is mended, and they are on friendly terms again.
Link travels north to the Twilight-covered Lanayru Province. He heads to Hyrule Castle Town, where he finds Ilia in Telma's Bar with a sick Zora child named Ralis. Link learns that Lake Hylia is facing a severe drought because no water is flowing from its source, Zora's Domain.
He heads up Zora's River with the help of the Twilit Carrier Kargarok, and finds Zora's Domain frozen. He and Midna ascend to the throne room and discover a large number of Zora trapped beneath the ice. They warp back to Death Mountain and transport a giant volcanic rock to Zora's Domain to thaw out the Zora and restore the water flow to Lake Hylia.
Before they leave, the spirit of the Zora Queen Rutela thanks them for saving the Zoras. She reveals that Shadow Beasts attacked Zora's Domain and executed her. She sent her son, Prince Ralis, to Hyrule Castle to inform Princess Zelda of their tribe's fate, but fears that something terrible happened to him. Rutela requests Link to save Ralis and promises to grant him the power to swim and respire in very deep water in return.
Link and Midna ride the flow of Zora's River down to Lake Hylia and meet the final Spirit of Light, Lanayru. Link collects the Spirit's Tears of Light to restore the light to Lanayru Province, eliminating the last of the Twilight from Hyrule. Lanayru informs Link that the final Fused Shadow rests beneath Lake Hylia and proceeds to tell Link a story about Interlopers who attempted to rule the Sacred Realm.
These individuals had mastered powerful magic and tried to control the Sacred Realm with it, but the Goddesses ordered the Spirits of Light to intervene. The Spirits sealed away the Interlopers' powerful magic into the Fused Shadow and banished them to the Twilight Realm. Lanayru warns Link not to be ruled by power and reiterates that the final Fused Shadow lies in the Lakebed Temple at the bed of Lake Hylia.
Link returns to Telma's Bar in Castle Town to reunite with Ilia, but finds that she has lost her memory and is distraught over Ralis' illness. Telma, the owner of the Bar, tells Ilia that she has heard of a Shaman in Kakariko Village who treats Gorons and Zoras. Link agrees to escort the trio to Kakariko Village. King Bulblin is revealed to have survived his fall off of the Bridge of Eldin, and Link once again battles him on the way to Kakariko, knocking him off the Great Hylian Bridge.
After crossing Hyrule Field and Kakariko Gorge and evading scores of monsters along the way, the group reaches Kakariko Village. Ralis is left in the care of Renado and the children, and Telma states that she will stay in Kakariko Village for the time being. After Telma leaves, Rutela's spirit appears to Link again and motions for him to follow her to Kakariko Village's Graveyard. She thanks Link for bringing her son to Kakariko Village and fulfills her promise to him by revealing the Zora Armor beneath her husband King Zora's grave. Rutela asks Link to tell Ralis that she wants him to not grieve her death and live on as king of the Zoras, and that she loves him unconditionally. After this final request, Rutela joins her husband in the afterlife.
Link heads to Lake Hylia with the Zora Armor and descends to the Lakebed Temple. After solving many puzzles in the dungeon, he defeats the aquatic creature Morpheel and acquires the final Fused Shadow.