A 104-102 comeback victory over the Utah Jazz secured the 73-year-old's 1,336th regular season win, surpassing the previous record held by Popovich's long-time friend, Don Nelson.
Into his 26th season and 2,030th game with the Spurs -- the only team he's ever head coached -- it was fitting that Popovich hit the unprecedented milestone courtesy of a thrilling fightback in front of a rapturous home crowd at the AT&T Center.
Having trailed by 15 points with 10 minutes remaining, the Dejounte Murray-inspired Spurs battled back to nudge ahead with a minute to go before a frenetic final 30 seconds saw a flurry of points from both sides.
Murray led scoring with 27 points, adding four rebounds and three assists, including the final point of the game courtesy of a free throw.
As the buzzer sounded, the point guard moved straight to Popovich to embrace his coach -- the pair sharing a hug before the new record holder was swarmed by his ecstatic players.
'All of us share in this record'
After finally breaking loose of the huddle, Popovich exited the court and moved to the media zone to reflect on an unprecedented achievement.
"It's just a testament to a whole lot of people," Popovich told reporters. "Something like this does not belong to one individual.
"Basketball's a team sport. You preach to your players that they have to do it together and that's certainly been the case in my life with all the wonderful players and coaches, the staff that I've been blessed with, the support of this wonderful city.
"All of us share in this record -- it's not mine. It's ours, here in the city."
Sharing a picture of the two embracing, Murray tweeted his appreciation for "the greatest coach of all time."
"You the greatest coach of all time and I'm thankful and grateful for you Pop," Murray said.
"I love you so much and you deserve this and can't nobody ever take this away from you!"
Friends at the top
A five-time NBA champion and three-time NBA coach of the year, 'Pop' had consolidated his legendary status long before his record-breaking feat was confirmed on Friday.
The outpouring of tributes in the wake of his achievement is a testament to the respect he garners across the league -- not least from the man he surpassed, Nelson.
Alongside Popovich in being one of only five coaches to win five championships, Nelson was one of the first to congratulate his "old buddy" in a video message tweeted by the Spurs.
"I just want to tell you how proud I am of all your accomplishments and the wonderful things you've done for basketball worldwide," Nelson said.
"I couldn't wait for this day to happen and I just want you to know that as one of my best friends in life I just wish you the best for your remaining years in the NBA."
Popovich served as assistant under Nelson at the Golden State Warriors in 1992, two years before his return to the Spurs.
Far from the flattering words his friend gave him, Popovich said he felt "undeserving" to be held in the same esteem as Nelson.
"The ironic thing about this is Nellie gave me a job when I didn't have one back in '92," Popovich said.
"He took me on. To be in this position, as the same breath as him, is in my opinion undeserving and quite awkward because he was so wonderful in saving my family's ass. So it's ironic that I'm sitting here in this situation."
'An amazing coach and an amazing man'
To commemorate the achievement, the Spurs have announced 'The 1336 Coach Pop Collection' -- a set of 1,336 NFT's each featuring a hand-drawn play from Popovich's tenure.
All proceeds from the collection will go towards the San Antonio Food Bank to help combat hunger in the area, the team said.
Meanwhile, NBA Commissioner Adam Silver praised Popovich for his "unprecedented" success in San Antonio.
"Gregg Popovich's success with the Spurs is unprecedented in our league so it's only fitting that he now holds the record for most career wins," a statement from Silver on Friday read.
"His leadership and unwavering commitment to the game are widely admired by generations of players and coaches alike."
A player under Popovich during two stints with the Spurs, Warriors coach Steve Kerr spoke to the people skills of his former mentor.
"Forget the wins, forget the record, all that stuff," Kerr said in a video tweeted by the Warriors.
"What is really meaningful to me and all of your former players is just what you've meant to us on a personal level -- how much you've helped us grow as people and the experiences you've provided for us.
"You are just an amazing coach and an amazing man."