Jonathan Ford will leave his position as chief executive of the Football Association of Wales on March 31 after losing the confidence of the FAW Council.
Ford's departure comes after the council passed a vote of no confidence in him by 26 votes to five on February 22, and at a time when there is uncertainty over the future of manager Ryan Giggs.
Wales will begin their 2022 World Cup qualifying campaign on March 24 with no chief executive and caretaker boss Robert Page in charge of the team in Giggs' continued absence.
An FAW statement said: "The FAW would like to place on record its gratitude to Mr Ford for his efforts over the past 11 years and wish him all the best for future endeavours.
"The FAW will not be making any further comment at this current time."
Ford was appointed FAW chief executive in 2009 and has been widely credited with lifting the association's profile and increasing turnover.
But the PA news agency understands there has been tension behind the scenes in Welsh football for the past 12 months.
It is understood that many clubs in Wales have been felt the FAW has failed to adequately support the grassroots game during the Covid-19 health crisis.
The restructuring of the FAW under Ford has also been an issue with councillors, while the appointment of Angela Van Den Bogerd as "head of people" in December 2020 caused friction.
Van Den Bogerd is a former Post Office director, who was found by a judge to have "obfuscated" and "misled" a court.
Ford worked as European Sports sponsorship director at the Coca-Cola Company before joining the FAW.
He led the governing body through a significant modernisation programme and was at the helm as Wales reached Euro 2016 – their first major tournament for 58 years.
Wales would go on to reach the semi-finals in France under manager Chris Coleman and a team that had often attracted a few thousand fans played before sell-out crowds.
Ford, a driving force behind the appointment of Coleman's successor Giggs, was also at the forefront of successful Welsh bids to stage the Super Cup final in 2014 and the men's and women's Champions League finals in 2017.
But Wales missed out on becoming a co-host of the cross-continent 2020 European Championships.
Ford's departure leaves Welsh football in crisis just 15 days before their opening World Cup qualifier against Belgium in Leuven and little more than three months before the delayed Euro 2020 tournament.
Giggs was arrested on suspicion of assaulting his girlfriend at his Manchester home on November 1 and the case file is currently under consideration by the Crown Prosecution Service.
Page took charge of Nations League fixtures in November, leading them to victories over the Republic of Ireland and Finland as Wales were promoted into the top tier of European football.