Brian Barwick is to leave his post as chief executive of the Football Association at the end of the year.
The decision was taken after weeks of discussion between FA chairman Lord Triesman and Barwick over his role within English football's ruling body.
Triesman is the FA's first independent chairman and has been responsible for looking at the way it is structured.
BBC 5 Live football correspondent Jonathan Legard said Barwick and Triesman's relationship had "crumbled".
"FA sources have acknowledged the chairman and Barwick have disagreed over the future direction of the organisation and the role of the chief executive," said Legard.
"His crumbling relationship with the chairman means he will have left well before the benefits are felt."
Wembley is a very different place from when I took over and I am very proud of that
Barwick said he hoped he would be remembered for securing the opening of the new Wembley Stadium.
"It's a very different place from when I took over and I am very proud of that," he said.
"If I have a genuine legacy, the stadium we were sitting in last night is probably one of the finest in the world."
He added that the FA's new Respect programme, an attempt to improve players' behaviour on and off the pitch, was "very special to him.
He could also point to the negotiation of a new £425m television deal for the FA and getting the green light for to the National Football Centre at Burton as other successes.
Most European countries have national football centres, but approval for Burton has taken the best part of a decade.
But as the fourth chief executive the FA has lost in less than 10 years, it is likely he will be remembered as much for the criticism the organisation received over the appointment of a successor to Sven-Goran Eriksson as England coach as any successes.
Barwick was spotted flying to meet current Chelsea manager Luiz Felipe Scolari, then in charge of Portugal's national team, but later said he had never offered the Brazilian the job when it Scolari made it clear he wanted to stay in Portugal.
And when Steve McClaren was appointed, Barwick's insistence that he had been the first choice all along was met with widespread scepticism.
The FA's insistence on appointing a manager before the start of the 2006 World Cup, thereby ruling out a number of candidates, also drew fierce criticism.
McClaren was not a popular appointment, and Barwick sacked him after England failed to qualify for Euro 2008.
BRIAN BARWICK FACTFILE
1980: Joins BBC from local newspaper
1995: Promoted to head of production at BBC
1996: Appointed head of television sport
1998: Moves to ITV after 18 years at BBC
2002: Renews Champions League contract for ITV
2003: Oversees broadcast of Rugby World Cuip
2004: Becomes chief executive of the Football Association
2008: Tenure at FA ends
His choice of Fabio Capello as McClaren's replacement was met with greater support.
Barwick added: "I have always endeavoured to do my job with passion, decency and integrity, and I believe I am leaving a strong legacy for the future.
"I'm a huge football person and to have been the chief executive of the FA was a very special thing.
"I'm really proud to have been able to do the job and I think we've moved the organisation on leaps and bounds and that's really important to me.
"This has been an absolute privilege to lead an organisation of this status and I'll take away a lot of warm memories.
"I also think in Fabio Capello we have got an absolute world-class coach."
Capello was diplomatic when asked for his reaction to Barwick's departure following England's laboured 2-2 friendly draw - a game watched by the chief executive - with Czech Republic at Wembley.
"It's not my problem, it's the board's decision," said Capello. "I'm a friend of Brian's and also of the chairman."
Triesman said: "On behalf of everyone at the FA, I would like to express my sincere thanks to Brian for the stability and growth that he has brought to the organisation.
"Brian leaves with our best wishes for the future, and will always be welcome back as our guest at Wembley."
A former editor of BBC's Match of the Day and producer of Football Focus, Liverpudlian Barwick was appointed by the FA in November 2004 three months after a sex scandal forced out his predecessor, Mark Palios.
Barwick quit his job in television as controller of ITV Sport to take up the FA position in January 2005.
Barwick had left the BBC in 1998 to join rival ITV, where he had helped secure coverage of the Champions League and 2003 Rugby World Cup.
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