This year, he's fighting to find a place to play.
Midway through his sophomore season in 2006, Holmes, a converted wide receiver, stepped into a starting role at cornerback, freeing up Reggie Smith to play safety as the OU coaches finally found a way to get their five best defensive backs on the field.
Holmes' performance stood out, especially with plays like the fourth-down pass deflection that put the Sooners in control of their 26-10 win at Missouri.
Once again, defensive coordinator Brent Venables and secondary coach Bobby Jack Wright are taking on the task of finding their five best DBs. "Certainly Lendy has established himself as one of those guys," Wright said.
But their decision to return Smith to cornerback pushed Holmes down the depth chart.
With senior free safety Darien Williams out for at least another week with a stress fracture in his foot, the coaches decided to experiment with Holmes at that position.
"It looked really natural," Venables said of Holmes' first experience at free safety. "(In the first practice) Lendy had a couple of picks without really knowing what he's doing yet.
"He played too well for us, made too many plays, to keep him off the field."
But that's not necessarily a guarantee of what's to come for Holmes.
Nic Harris is the current free safety starter, with Holmes sliding into that spot and Harris playing closer to the line in five-defensive back situations. But when Williams returns, Holmes gets bumped again.
Holmes maintains a relaxed attitude about the position change and what could be a significant drop in playing time.
"I'm just playing wherever they tell me to play," he said. "I'm learning everything. I feel comfortable with myself. But I still have a long way to go."
That mostly entails learning the added duties of the safety position.
"A lot more responsibility," Holmes said. "Learning when I'm in the run fit, when I'm not. Learning when to blitz. It's a lot, but it's slowly coming to me.
"Coach Wright ain't yelling at me that much yet."
Holmes still knows the cornerback position well enough to step in if needed, but he's focusing all of his attention at free safety in training camp. And he seems to enjoy the opportunity to be more physical at his new home.
"I'm just waiting for somebody to come across the middle now," he said.
