The Walton-Penner Ownership Group agreed to pay $4.65 billion ($A6.65 billion) - a record price for a sports franchise - to settle the purchase from the Bowlen family. The late Pat Bowlen, and his heirs, had owned the team for 38 years.

The two sides agreed to the deal in June.

"We are grateful for the support and trust of the National Football League and the 31 other teams with today's vote. We couldn't be more excited to join the Denver Broncos," Walton said in a news release Tuesday.

"It's a responsibility and privilege to serve as stewards of such an iconic franchise. We have tremendous respect for what Pat Bowlen has meant to the Broncos and look forward to building on this organisation's championship legacy."

Forbes pegs the net worth of the 77-year-old Walton at $65 billion ($A93 billion), putting him in 19th place on the publication's list of billionaires. He is the richest owner in the NFL, with only Steve Ballmer of the Los Angeles Clippers worth more among North American sports teams.

The previous record sales price for an NFL franchise was the $2.275 billion ($A3.25 billion) David Tepper paid for the Carolina Panthers in 2018.

Walton's ownership team also includes his daughter, Carrie, and her husband, Greg Penner, as well as notables such as Condoleezza Rice, former secretary of state, and Formula One driver Lewis Hamilton. The Penners are expected to lead day-to-day operations.

Rob Walton now becomes the second NFL owner from the extended Walton family. Ann Walton Kroenke, who is Rob Walton's cousin, is married to Stan Kroenke, owner of the Los Angeles Rams.

And they can have a family reunion, of sorts. The Kroenkes also own the Colorado Avalanche of the NHL and the Denver Nuggets of the NBA.

Australian Associated Press