Widowmaker is first introduced crossing a desert with vultures circling above him. The young horse tries to defend himself but is quickly overwhelmed due to his thirst. However, Bill arrives in time and saves Widowmaker from the vultures. Since then, the pair became inseparable.
In the years that followed, Widowmaker and Bill accomplished many achievements, from lassoing evil rustlers, to digging up the Rio Grande and creating the Painted Desert. One day, as they were butting heads with buffalo, they meet the beautiful redheaded cowgirl Slue-Foot Sue, who immediately captures the attention of Pecos Bill whilst riding on her giant catfish down a river. Bill's eccentric behavior confuses Widowmaker at first until he realizes that the cowboy has fallen in love with the young girl and starts to cry. During that evening, as Bill successfully woos Sue, Widowmaker weep over the thought of losing his closest friend.
On Bill and Sue's wedding day, as Bill excitedly waits for Sue, several other cowboys with ropes are holding down Widowmaker, who is now in a fit of jealousy over Sue taking Bill away from him. When Sue sits on his back wearing her yellow gown and bustle, he attempts to throw Sue off. Surprisingly, Sue is able to stay on Widowmaker for a while, despite him bucking so much that his horseshoes come off. But while Sue calmly powders her face during her rough ride, her bustle suddenly begins to bounce repeatedly. Widowmaker continues to buck Sue's bustle, sending her higher and higher until the leather reins tear in half.
As Sue bounces up into the sky over and over again, Bill attempts to lasso her down. Unknown to Bill and the others, Widowmaker stands on the rope whistling innocently, causing Bill to miss and Sue to land on the moon. After that, Bill and Widowmaker return to the coyote pack.
Widowmaker makes a cameo appearance in "This is Your Life, Donald Duck" of this series along with some other characters.
- He bears a striking resemblance to Cyril Proudbottom from The Adventures of Ichabod and Mr. Toad.
- He is the first hero's horse who is jealous of the hero's love interest. The second is Pegasus from Hercules.
- In some versions of the tall tale, he is referred to as Lightning.