After March 29, when Britain and the North of Ireland exit the European Union, the Candystripes will be only club in the UK still plying its trade within the remaining 28 EU states.
The outskirts of Derry straddles the border with Donegal.
But after Brexit, it will straddle the new EU-UK frontier.
The club’s Ryan McBride Brandywell stadium is just four miles from its neighbouring Donegal.
And for the past 34 years they have played in the League of Ireland.
Derry City FC will not be drawn on how Brexit might affect the club post Brexit.
However, the Republic’s government is planning for how cross-border sports could be impacted by Britain’s EU withdrawal.
“Sport Ireland is the main statutory organisation that liaises with Ireland’s national governing bodies of sport, including those 46 bodies that operate on an all-island basis,” said a spokesman for the Department of Transport, Tourism and Sport.
“Both the Department and Sport Ireland acknowledge that the uncertainty of Brexit may pose challenges to all-island national governing bodies and remain available to assist such organisations should this be required.”
In 1972, during one of the worst years of the Troubles, a bus carrying supporters of Ballymena United was burned during a visit to Brandywell.
As a result, the Irish Football Association expelled Derry City from the Irish League.
It wasn’t until another 13 years later in 1985 that the club was accepted into the League of Ireland.The Government may be planning for all possibilities but fans are thinking only about football.
Mickey Kerrigan, chairman of the Pride of Northside supporters club, who has been travelling home and away to matches since 1985, says politics should not interfere with football.
He told BBC NI News: “People can make all the predictions they want about Brexit, but the truth is that no one knows what will happen.
“Derry City fans have already been through the years of a hard border, we’ve had traffic tailbacks, delays and checks on the border and we shrugged our shoulders and got on with it.
“I can’t see what change there will be for supporters, maybe some traffic issues if anything, but we have a new manager, new signings and are ready to get on the road for the new season,” he said.
Derry City begin its 2019 League of Ireland campaign at home tonight, February 15, against UCD (kick off 7.45 pm) under new manager Declan Devine.
On March 29 – the official Brexit date – the Candystripes host Sligo Rovers at the Brandywell.