Conservative Cllr Terry Freer, who represented St Peters, has stood down having first been elected in 1976.
In a letter to fellow councillors, Mr Freer said: “I wanted to drop you a line to let you know that I have decided that it is time for me to retire from the borough council.
“That has not been an easy decision to reach but it is one I know is right.
“Over many decades I have enjoyed the company and support of councillors of all parties and of our officers.
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“There have been times where we have not all agreed but that is inevitable because of the passion we feel for the borough and its citizens.
“I owe a special thanks to my ward councillor running mate, Mary Malin, who has been a friend and confidant for more years than both of us would care to remember.
“I am not vanishing and will no doubt bump into people, but I think it is time for me to pass on the baton to someone else while I enjoy more time with my family.”
The council plans to mark Terry’s long service to the community at a future council meeting.
A Kettering Council spokesman confirmed that there would be a by-election after Cllr Freer’s resignation on March 24.