Sir Clive Booth, chair of the Big Lottery Fund, is to stand down after seven years in the role.
A spokeswoman for the Big Lottery Fund said Booth handed in his resignation to Ben Bradshaw, who was then culture secretary, on 31 March. He will leave the position at the end of November.
"By giving his notice in March, Sir Clive hoped that the Department for Culture, Media and Sport would have enough time to recruit and appoint a new chair and ensure a smooth transition," she said.
Booth apologised to the Conservative Party in 2008 after he accused it of being "hostile to the voluntary sector" and said he thought it needed a "seminar in elementary arithmetic".
Jeremy Hunt, now culture secretary, was in the shadow role at the time and complained to cabinet secretary Sir Gus O’Donnell about the comments. Booth subsequently issued an apology.
The DCMS has begun the recruitment process for Booth’s replacement and advertised the position on its website.
The appointment will be for an initial period of up to four years and will require an average of six days’ work a month. The salary has not been set, but Booth was paid £39,728 in 2009/10.
The closing date for applications is 15 September.