Councillor Dominic Nolan, who represented the Tories in St Andrews, is understood to have stepped down for work reasons after serving just over four-and-a-half years as a local member.
Opposition councillors have reacted angrily to the timing of the move as it means no by-election will have to take place because the next local elections are fewer than six months away.
The 26-year-old, who was elected in 2017 with a 20% share of the vote, confirmed he has resigned, but declined to comment further.
Liberal Democrat councillors in Fife have now branded Mr Nolan’s resignation a “sign of diminishing Tory presence” in the region, suggesting his decision to hold on to the job until just within the six-month deadline has prevented a by-election from taking place in the ward where - they believe - the Conservatives would lose their seat.
Lib Dem group leader Tim Brett said: “The strength of the Conservatives in North East Fife has been diminishing for years and this resignation makes them even weaker.
“People know that only the Liberal Democrats stand up for our local communities and are capable of winning from the SNP here.”
Jane Ann Liston, local Lib Dem councillor for St Andrews, added: "Our strong local team of councillors work all year round, not just at election time. We listen to what people need, take action and report back with local newsletters.
“This resignation, and the decline of the local conservative presence, just goes to show that we are best placed to stop the SNP and their plans to push the cause of independence, including through Fife Council.”
However, Fife Conservative group leader Dave Dempsey stressed there was nothing untoward about the timing of the announcement.
“He’s got himself a job and to be honest he’s got to think of his future,” he noted.
“You can’t build a career as a councillor, and you can’t ask someone like Dominic to live on £16,000 a year with potentially the threat of redundancy every five years.
“If it was a single member ward then I could see the point, but it’s a four-person ward and there are still three councillors if somebody needs to find one - it’s not as if we’re leaving the public bereft.
“It would actually cost the public purse more to hold a by-election.
“I can’t imagine the public would be delighted with the prospect of going out to vote in January or February for someone who might not even last the induction period.”
The resignation leaves St Andrews with three councillors until the next election in May, namely the Lib Dems’ Jane Ann Liston, Labour’s Brian Thomson and the SNP’s Ann Verner.