The former Northampton South MP became general manager of the club in 2005 after five years on the board in a supporting/non-official role.
He then took up a part-time director role in 2008 before coming off the pay roll in May this year.
"I still love this club with a passion, but sometimes you have to move on to help freshen things up," said Clarke.
"I also want to simply be a fan again and go to games on a match day in my jeans and watch the game."
The local independent borough and county councillor, 46, is still keen to help the club with their plans to re-develop the Sixfields Stadium, something chairman David Cardoza has said would be put on hold in the current financial climate.
"My decision to step down from the board might not be so welcome at the Town Hall," said Clarke.
"Because of the conflict of interest I was always denied the opportunity to speak on the subject of the re-development when it was raised in debate.
"Now the gloves can come off and I can tell them a few unwelcome truths as to how successive councils have let the club down."
Cardoza added: "Tony is Northampton through and through and will continue with the good fight for NTFC.
"I am very happy with the make-up of the board. Everybody involved has a passion to bring success to NTFC both on and off the field."
The Cobblers board is now made up of Cardoza and his father Tony, Barry Hancock, David Jackson, finance director Barrie Egan, supporters representative Anthony Collett and company secretary Norman Howells.
Source: BBC Sport
Source: BBC Sport