When the Legends Die traces the life path of the novel's protagonist Thomas Black Bull, a Native American Ute from Southwestern Colorado. As a young boy, Tom lives with his mother Bessie and his father George Black Bull in Pagosa. However, when George Black Bull kills Frank No Deer for having repeatedly stolen money from him, the family must flee the town. Returning to the wilderness, they live happily in the old Ute way. One winter day, an avalanche kills Tom's father as he hunts in a valley. Tom adopts the name "Bear's Brother," as well as the role of the man of the family. When Bessie returns to Pagosa to visit the general store, she learns that her husband's name has been cleared but still hesitates to move back into town. The following winter, Bessie becomes ill and dies. Living alone in the wilderness, Tom befriends many animals and becomes particularly close to a bear cub whom he considers his closest friend and his brother.

When another Ute, Blue Elk, approaches Tom, allegedly to encourage him to spread knowledge of the old Ute ways to the townspeople of Pagosa, Tom agrees to travel there. His bear accompanies him on his journey. However, Blue Elk forces Tom to attend the local reservation school, where Tom becomes angry and depressed, and where the teachers chain the bear to a fence. Blue Elk soon tricks Tom into believing he will be released, but they journey into the mountains solely to release the bear. After numerous unappealing classes and jobs, Tom meets a man named Red Dillon during a trip to the town of Bayfield. Red, impressed with Tom's ability to ride a wild bronco, convinces him to return to his ranch with him to better his riding skills.

After some training at Red's ranch, Tom and Red travel to countless rodeo competitions, at which Tom demonstrates his skill. But, Tom must obey Red's instructions to ride in a way that will benefit Red's betting efforts. Over the years, Tom becomes increasingly frustrated with Red's control over him, as well as Red's drunken and obnoxious behavior, and soon Tom asserts his independence from Red. After his competition has finished, Tom drives Red back to his ranch. In the fall Red wants to take a trip with Tom, but Tom refuses to accompany him; nonetheless, Red soon departs. A stranger comes to Red's ranch to inform his Mexican cook, Meo, and Tom that Red has become very ill. Rushing to his aid, Tom travels to the hotel where Red is staying in order to care for him. However, Tom cannot even carry Red to the car before Red dies in Tom's arms.

Returning to his rodeo life, Tom enters the professional circuit, where he continues to exhibit his skill and brutality, developing a reputation as "Killer Tom Black." When Tom returns to Red's old ranch to visit Meo, Meo shows little interest in conversation and seems to act oddly; Tom leaves promising to return shortly. During a particularly brutal ride Tom breaks his arm, and leaves the hospital to visit Meo once again. Arriving at the cabin, Tom finds Meo absent and later learns from a doctor in town that Meo has died a few weeks prior. He falls into an even deeper despair, having lost many people in his life. His riding style becomes increasingly abusive, and his social behavior increasingly reclusive. During a ride at the Garden in New York City, Tom becomes seriously injured in a fall. Nursing his injuries at the hospital, Tom receives advice from his doctor that he should never ride again, but he remains determined to return to the ring. His nurse Mary Redmond treats him with care and kindness, but he resents her efforts and believes she simply wants to control his life, as so many other individuals have tried before her. Having regained his ability to walk after significant efforts, Tom leaves the hospital with only a curt goodbye from Mary. He heads west on a train to his homeland.

In Pagosa, Tom feels self-conscious and assaulted by many memories of his younger life there. In the general store, he meets Jim Woodward, who offers him a job as a shepherd in the mountains. He decides to work as a shepherd for a while. During his time in the mountains, Tom has the necessary time and space for his thoughts. Contemplating his past and the meaning of his life, Tom first begins to recognize his poor treatment of both animals and other people. He also begins to process his painful memories and to come to terms with them. One day a bear emerges from the woods and kills one of the sheep; Tom reacts by yelling at it to run away. Later he regrets not having killed the bear and regards his hesitation to shoot it as foolish. Returning to town with Jim, Tom gathers supplies at the hardware store before packing his bag and heading back up to Horse Mountain unobserved. There he intends to kill the bear that has killed the lamb. However, when he finally spots the bear once again, he aims his rifle at it but finds he cannot pull the trigger. In his dreams the All-Mother appears and defends him from the fury of nature's element, claiming Tom as her son. Tom leaves the bear alone and engages in the old Ute ways. The novel ends with his contentment in his solitary life in the wilderness and in the ways of his heritage.