Previously, he served as the head coach of the New Orleans Saints from 2006 to 2021, leading the franchise to its first Super Bowl victory during the 2009 season.

Payton has always been known for his offensive prowess, having scored more points (2,804) and gained more yards (40,158) than any other team in a coach's first 100 games in NFL history.

Under Payton's leadership, the Saints made the 2006 NFL playoffs after a 3–13 season in 2005 and advanced to their first NFC Championship appearance in franchise history.

Winning a football scholarship, Payton had a successful career playing quarterback at Eastern Illinois University, leading the Panthers to an 11–2 record and the quarter-finals of the Division I-AA Playoffs in 1986.

[26] In 1998, Gruden and Callahan left for the Oakland Raiders, and Eagles head coach Ray Rhodes and Payton were fired.

Payton recalls this moment in his autobiography Home Team: Coaching the Saints and New Orleans Back to Life.

[32] During the 2002 season, after several poor showings by the Giants' offense, Payton's role in play-calling was taken over by then head coach Jim Fassel.

However, Payton turned the struggling team around, and, with newly acquired free agent quarterback Drew Brees, led them to their first playoff appearance in six years.

Receiving 44 out of 50 votes from a panel of sports journalists and broadcasters, Payton won the AP NFL Coach of the Year Award in January 2007.

In June 2010, Payton published a book (written with journalist Ellis Henican) entitled Home Team: Coaching the Saints and New Orleans Back to Life.

In a memorable moment the week after, Payton was spotted eating a hot dog in a relaxed state while the Saints blew out the Indianapolis Colts 62–7.

When informed that the league was investigating reports of a bounty program, Payton met with Williams and assistant head coach Joe Vitt and told them, "Let's make sure our ducks are in a row.

[43] On March 22, 2012, NFL Commissioner Roger Goodell suspended Payton for the entire 2012 season, effective April 1.

For instance, during its investigation, the league uncovered an email that Michael Ornstein, the agent for former Saints running back Reggie Bush, had sent to Payton.

"Ornstein's email is just another example of the speciousness of the quote-unquote evidence that Commissioner (Roger) Goodell claims to have to support his erroneous accusations against Jonathan and the other players," lawyer Peter Ginsberg said.

Goodell held an expedited hearing on the matter and was expected to render a decision in "days, not weeks," according to ESPN's Schefter.

[52] Soon after the suspension was announced, Payton began discussions with his mentor Bill Parcells about serving as an interim coach for the 2012 season.

[10] During his 2012 suspension from the NFL, Payton served as the offensive coordinator for his son Connor's sixth-grade team in Argyle, Texas.

Since he believed he would face that team again in the league's playoffs, he obtained video that the father of one of his players had recorded, and then contacted his mentor Bill Parcells to help him break down the opponent's offense.

But on the last play of the game, Vikings quarterback Case Keenum threw a 27-yard pass to wide receiver Stefon Diggs, who evaded Saints safety Marcus Williams and ran to the end zone to complete a 61-yard touchdown pass as time expired to win the game for Minnesota, 29–24.

The game was marred with controversy after the referees missed a pass interference call of Rams cornerback Nickell Robey-Coleman's hit on Saints wide receiver Tommylee Lewis on 3rd-and-10 with 1:45 remaining in the fourth quarter.

The fallout from the missed call was a factor in the NFL's decision to expand instant replay, making pass interference (including non-calls) reviewable.

[62] On February 28, 2022, it was revealed that the Miami Dolphins had requested permission from the Saints to interview Payton for their vacant head coaching spot, but were reportedly denied permission and had scrapped the idea after their former head coach, Brian Flores, filed a lawsuit against the NFL over racial discrimination in hiring practices early that month.

The Dolphins were considering pairing Payton with quarterback Tom Brady, who had briefly retired from the NFL from February 1, 2022, until March 13, 2022.

[66] Six months after the pursuit was first reported, on August 2, 2022, the Dolphins and team owner Stephen M. Ross were fined $1.5 million and forfeited a 2023 first-round draft pick along with a 2024 third-round pick due to impermissible communication with both Payton and Tom Brady, who both share the same agent, Don Yee, between the 2019 and 2021 seasons.

[68][69] In January 2023, Payton interviewed for head coach vacancies with the Denver Broncos, Carolina Panthers, Arizona Cardinals, and Houston Texans.

[70][71][72][73] On January 31, 2023, Payton reported that he had accepted the position of head coach for the Denver Broncos, and was officially hired three days later.

[78][79] In Week 18, the Broncos, with Payton as the head coach, clinched their first playoff berth since the 2015 season after defeating the Kansas City Chiefs 38-0.

[89] Rumors swirled over the 2011 Super Bowl weekend that the move would coincide with Payton returning to the Cowboys as the General Manager or in some other executive capacity, but these turned out to be groundless.

[94][95][96] Saints running back Alvin Kamara had recorded the locker room celebrations for his Instagram live feed and the video went viral on social media.