Shaun Harvey will leave his role as chief executive of the English Football League at the end of the season.
Harvey, 48, took over as CEO in 2013 and has been involved in football for 25 consecutive years.
He said he was proud of what he has achieved "in what have not always been easy circumstances".
Harvey oversaw a controversial deal for domestic broadcasting rights, which several Championship clubs said left them "gravely concerned".
The unhappy clubs claimed the £595m five-year agreement with Sky Sports, which was signed in November 2018 and represented a 35% increase on the previous contract, had been done without them being fully consulted.
During Harvey's spell at the EFL, member clubs have sought to address the under-representation of Black, Asian and Ethnic Minority (BAME) coaches, while he strongly supported calls to introduce safe-standing areas at football grounds.
Harvey added: "Consistently during my time, I have always looked to push boundaries to make the maximum positive impact for clubs, whether this be from a financial perspective or by generating value in another way.
"I have always held the view that the strength of the EFL is its clubs and no club, or indeed individual, is bigger or more important than the collective or the EFL itself.
"The time is right for the EFL to move in a different direction having concluded a number of commercial contracts that leave the League in a stable position."
Debbie Jevans, interim chair of the EFL said: "The EFL would like to thank Shaun for all he has delivered. The EFL is in a strong position with a growing fan base throughout the world and Shaun deserves a lot of credit for this."
FA chief executive Martin Glenn, who will also leave his post at the end of the season, added: "On behalf of the FA, I would like to thank Shaun for his leadership of the EFL and his collaborative support over the years.
"The EFL and its clubs play a crucial role in English football and its popularity has flourished during his tenure. Shaun's redesign of the Checkatrade Trophy has been a valuable tool for giving game time to young English talent from our academy system."
Harvey joined the EFL after nine seasons as chief executive at Leeds United. Before that, he had a decade at Bradford City, having started his career in football in 1992 as secretary at Scarborough.
Simon Stone, BBC Sport
Harvey has been on borrowed time since November, when he agreed the new TV deal.
Not only did the majority of Championship clubs feel the deal undervalued the rights, but they were furious at the fact it gave away the streaming rights to matches taking place away from the normal Saturday 15:00 slot, when many of them felt it was a method of generating additional revenue for themselves.
Although Harvey rode out that storm, he had lost the confidence of the Championship clubs, which effectively meant he was condemned to enduring a continued difficult relationship for as long as he remained in post.
A controversial figure, who was also responsible for the hugely contentious decision to invite 16 top-level under-21 sides into the Checkatrade Trophy, it remains to be seen what Harvey will do now.
But the senior EFL clubs will be looking for a replacement they feel acts more in their interests.