Holmes becomes the second Black general manager in team history, following Martin Mayhew, who was the team's general manager from 2009 to '15.
The Rams will become the first team to receive two third-round compensatory draft picks as part of the NFL's new hiring initiatives.
"Several weeks ago when we embarked on this process, it was critical that we find the right person to fit our vision for this team," Lions owner Shelia Ford Hamp said in a statement.
"It was evident early on that Brad is a proven leader who is ready for this opportunity."
Holmes initially interviewed with Detroit virtually on Jan. 6 and then in person Wednesday. The North Carolina A&T grad -- he majored in journalism and mass communication -- has spent his entire professional career with the Rams.
He began as a public relations intern in 2003 before moving over to the scouting side and working his way up to his role as the director of college scouting. Now, he'll be replacing Bob Quinn, who was fired by the Lions in November after almost five years in the job.
Among the players taken during his tenure as the Rams' director of college scouting were two-time NFL Defensive Player of the Year Aaron Donald, wide receiver Cooper Kupp, safety John Johnson III, linebacker Samson Ebukam, tight ends Tyler Higbee and Gerald Everett, running back Todd Gurley and quarterback Jared Goff.
"The standard is, first of all, we get passionate players," Holmes told the team's website in 2019. "We talk about being good teammates, being a connected team. We talk about being relentless. We want smart players, instinctive players, explosive players.
"Those are the kind of pillars that we look for in football players for the Rams. You're smart. You're instinctive. You're explosive. Those are the core components, critical factors that we look for."
We just got off a great emotional call with Brad Holmes that of course ended with Les and Brad breaking down the draft... which led me to ask Les when he first knew Brad had "it"... .@Lions fans - get jacked... he's built for this!(oh and comment at end🤣) pic.twitter.com/AquGmgQwjJ— KHS (@KaraHenderson) January 14, 2021
The 41-year-old Holmes could alter his vision now that he's in the general manager seat since he does have experience under five head coaches and four general managers during his time with the Rams, but Holmes hit a lot of the things Detroit searched for in the process.
"We think in some cases very unique to our situation," Lions team president Rod Wood said recently. "I won't share all of them with you, but I would say they focus on leadership, culture, teamwork, awareness of each other's strengths and weaknesses, and what we're really looking for is a culture that is open, inclusive, where everybody is pulling together as a team, and in one word, communication is paramount and everybody is doing the right thing for the Detroit Lions.
"So, the people that we're looking for and the people that we're bringing in to interview, I think, exhibit those traits."
Rams general manager Les Snead told ESPN's Lindsey Thiry that Holmes has "dynamic intelligence" and that he respected his ability to evaluate football players. The team's chief operating officer, Kevin Demoff, told Thiry he also was able to be a leader away from the machinations of football.
That is something Wood harped on when he described what the team was looking for -- someone to lead and unify the organization across all levels.
Holmes is the nephew of Luther Bradley, Detroit's first-round pick in 1978, and the son of former Pittsburgh offensive lineman Mel Holmes.
"He's become a valued voice in our organization as part of our leadership team on social justice and diversity issues, helping us lead a diverse group of people," Demoff told Thiry. "Brad is one of the more valued voices we have in our building."
The Lions had been at the forefront of diversity issues in the NFL over the past year. They were the first team to protest the shooting of Jacob Blake in August by canceling practice the day before the Milwaukee Bucks refused to play a playoff game in protest of Blake's shooting.
Ford Hamp had a Yale classmate, Dr. Henry Louis Gates Jr., speak to her team virtually in August. Gates Jr. is the director of the Hutchins Center for African and African American Research at Harvard and the host of the PBS show "Finding Your Roots."
The Lions interviewed at least 12 people for the vacant position, including their three internal candidates and former general managers Rick Smith (Houston), Thomas Dimitroff (Atlanta) and Jeff Ireland (Miami).
Holmes will report to Ford Hamp and Wood.