It is known that Watmore had a number of disagreements with Sir David Richards, the chairman of the Premier League.
Richards has admitted there had been differences of opinion, but viewed those as the rough and tumble of football politics.
BBC Sports Editor David Bond learned that Watmore's frustrations were exacerbated by Saturday's e-mail leak to a national newspaper.
The e-mail mentioned details of a briefing given to the FA board and other senior association figures on the appointment of new marketing and communications director Julian Eccles.
In response, Watmore sent an angry e-mail to everyone who had been briefed, including the 12-man FA board, at 1710 GMT on Saturday.
The BBC has obtained details of the e-mail, in which Watmore wrote: "I don't know which sad person thought to brief yesterday but we know it had to be from this list as you are the only people who received it.
"I have three things to say: There's not a cigarette paper between me and the [FA] chairman on any issue and he is a man of ethics, character and courage, rare in my experience of any walk of life let alone football.
"If I ever find the person who leaked the briefing then I will ensure that that person's reputation is damaged beyond repair. This is the last time I share any information in advance."
BBC's sports news correspondent Gordon Farquhar suggested the leaked e-mail could have been the "straw that broke the camel's back" for Watmore.
"He wanted to leave a legacy of better governance within the FA and he had a five-year plan," said Farquhar.
"That he has gone after just nine months suggests that he had an enormous amount of frustration.
"The FA is not set up like a commercial organisation - where there is an executive board, where people make decisions and get on with things.
"It is a system of committees where you need to have a consensus and people need to be brought in to agreement before decisions get into the board and maybe that is what he found most frustrating."
Watmore, who came to the FA from the Department for Innovation, Universities and Skills, succeeded Barwick, who left the FA at the end of 2008.
You cannot tell me what the agreed priorities of English football are - neither can I and I worked there for 13 years
Former FA executive director David Davies
Barwick was preceded by Graham Kelly, David Davies (in an acting capacity), Adam Crozier and Mark Palios.
Following this latest blow to the FA, Davies, a former FA executive director, says there needs to be reform of the governing body.
"The reality is that most of these chief executives have been victims, and it seems Watmore is merely the latest, of the chronic instability inherent in the way English football is run," he told BBC Radio 5 live.
"That structure builds-in conflict which is hardly surprising given it is riven by conflicts of interest and people's roles and responsibilities are either not defined at all, are blurred, or worse still, set up directly in competition with each other.
"The past generation, my own generation, has failed to find a way forward for the whole game.
"You cannot tell me what the agreed priorities of English football are - neither can I and I worked there for 13 years."
In 2005, leading civil servant Lord Burns was commissioned to review the FA's structure following a series of scandals, including the resignation of Palios following newspaper allegations concerning the then England coach Sven-Goran Eriksson's affair with former FA secretary Faria Alam.
Following the report, Triesman was named as the FA's first independent chairman in 2007.
The FA governs and regulates all levels of the game, claiming it invests £38m into grass roots football.
It runs 24 England teams and 11 competitions, including the FA Cup, and developed the new Wembley Stadium.
The other members of the FA board are Premier League chairman Richards, Manchester United chief executive David Gill, Bolton chairman Phil Gartside, Ipswich chairman David Sheepshanks, Barnet chairman Anthony Kleanthous, Barry Bright of the Kent FA, John Ward of the Hampshire FA, Roger Burden of the Gloucestershire FA, Michael Game of the Essex FA and Dave Henson of the Devon FA.
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