Wolf Quest starts out with Balto having a nightmare about going on a journey. His dreams start with him following a raven through a field of ice, and running into a wolf pack. After being rudely awakened by Boris, Balto and the goose go into town to visit Jenna. They soon walk by a Totem Pole and Boris tells Balto it has something to do with his dreams, but he just shrugs it off. When they arrive in town, they soon found out that Jenna has just had puppies! All of them pretty much look like her, except for one gray-coated pup that looks much more like Balto. Time passes and soon all of the puppies are adopted and given away to good homes, except for the gray-coated one, Aleu.

With a heavy heart, Balto tells Jenna that no human is ever going to want her because she looks so much more like a wolf. Jenna just said that they will have to keep trying. Soon the 8-week-old Aleu is now 1 year old, but no one has adopted her. However, Balto still holds out hope. Until one day, a human hunter mistakes her for a wolf, and she narrowly escapes death thanks to Balto, Boris, Muk and Luk. Balto is forced to tell Aleu the truth, and she is horrified that she was part wolf. Balto’s mother is a white wolf, while his father was a husky, he explanes to Aleu. But, Aleu runs off to find out who she is, while Balto when after her in the hopes of bringing her home. Jenna, Boris, Muk and Luk stayed out of this adventure as Boris realizes that this is one of those father and daughter moments and added that they will be safe because thay are both part wolf!

Aleu quests to find out who she is, while Balto faces all kinds of challenges along the way. Aleu meets a mystic mouse named Muru who tells her that she has to keep looking and have faith and trust in herself to fine out who she really is. When Balto and Aleu are together again , they had to fend off a bear to keep themselves alive. Aleu gains an Inner Knowing from the bear and tells her father that they must jump off the steep cliff in order to save themselves. Balto is more that reluctant, but Aleu pushes him off, and jumps off too. Instead of falling to their deaths, they land on a ledge. She knew the ledge was there without seeing it!

Balto tells her daughter that it is time to go home, however she refuses to go until she finds out who she is. Balto decides to accompany her, and Aleu was touched by her father. Unfortunately, after reaching a rocky shore, three wolves lead by Niju, attacked them. Aleu and Balto decide to take on the three wolves. However, the fight breaks up quickly with the coming of the tide, and everyone runs for safety to avoid being drowned. Niju ordered them to keep attacking. Suddenly, the whole wolf pack appears on the shore, and the true leader, awise old wolf named Nava, orders Niju to stand aside. Niju finally let Balto and Aleu pass, and the two finds out that Nava had been waiting for them.

Nava tells the pack that the caribou (a dear like creature that mainly lives in Alaska) will not be returning for the winter, nor any other winter. They must cross the sea to an island to follow the caribou or die from starvation, and Balto will have to lead them! When Balto is reluctant to accept, Niju takes the opportunity to sway the pack away from Nava. Aleu steps up and directly challenges Niju by calling him a coward. Niju tells everyone that it is impossible to swim across the sea to the island. Everyone who believes Niju follows him. Balto tells Aleu that this has gone too far and they both are to leave for home the first thing the next morning. During the night, Aleu had sa dream about caribou crossing patches of ice.

The next morning, the wolf pack lead by Niju prepare to strike other wolf packs and steal food from them. But he was cut off by Balto, who had changed his mind. Just when Niju and the pack are about to attack Balto, Nava notices that the ice-breaks in the sea are lining up to form a bridge, one that extents all the way to the island. Aleu tells everyone she had a similar dream and Balto confesses he also dreamed of the caribou. Nava warned that when the time to cross the sea comes, they would have to take it immediately.

Everyone pushes Niju aside, who is bent on staying, and they all prepare to cross the ice blocks. Balto lead them across, while Aleu and Nava bring up the rear. Unfortunately, the ice block that Nava is standing on, breaks off and he drifts away from everyone else. Aleu joins him and offers to help, while she tells her father to keep going,and he wishes her luck. However, Niju is still furious and tries to kill Nava. Even though Aleu comes to his rescue, she isn’t strong enough to stop Niju. Just when he is about to put a serious hurting on Aleu, Balto steps in again. Niju was shocked that Balto was able to swim so far, so fast, and he backs off. However the wolves on the ice block are left without a leader, and are clueless as what to do. Balto offers to help Nava swim over to the wolves, but he refuses, knowing that he will not be able to make it. Balto then gives Niju a chance to lead the pack, but the rouge wolf was overwhelmed by the responsibility and by leaving home. He runs off back to the shore.

Balto tells Aleu to watch over Nava while he leads the pack, but Aleu tells him that he does not belong in the wild, while she does. Nava agrees, and admits that the one who is wolf but does not know was not Balto, but Aleu. Balto was hard with having to leave her daughter but they had to say their goodbyes, and before leaving, Aleu tells Balto to tell Jenna not to worry as she has finally found her home. With one final nuzzle, Aleu swims off to lead the pack. As she goes, Balto remembers Aleu when she was a pup. Once she reaches the large ice patch, she was pulled onboard. She howls goodbye to Balto, while the rest of the pack join in as they float away.

Nava assures that Aleu will make a great leader, and then runs off to find Niju. When Balto was about to head back for home, he was greeted by his mother, the white wolf, Aniu. After a goodbye howl, Aniu takes her leave, and disappeared as mysteriously as she came. Balto says goodbye to his mother before beginning his journey back to home.