Now it's time to see if he can handle a major workload, carrying the ball 20 or 25 times a game.
“The backs that we have had in the past have all carried the ball that many times,” said Cowboys coach Mike Gundy.
“He has done really well for us over the years, and he is ready to take the workload this year.”
Smith has earned his shot, coming a long way from the time early in his career when he wasn't sure he wanted to remain a part of the program, even going home to Tulsa for a few days to contemplate his future.
And the Cowboys need Smith to make the most of his shot.
“Jeremy Smith is kind of the war daddy, the old guy,” Singleton said. “He's a sixth-year guy who's been around the block a bit. He knows it. He's played it. He's been the backup and now he's got a chance to step into that starring role.”
Smith understands he can't relax now that his time has arrived.
“I know I have to go out with the mindset knowing I'm the guy,” Smith said, “which means I have to work harder than any other running back out there, because they believe in me and I believe in myself, too.
“I've had my opportunities. And I'm blessed to be a part of this knowing it's my turn now.”