By 1988, O'Mahony was re-installed as manager, and the side finished eighth in the league, and a loss to champions Derry City in the FAI Cup final earned the club its first European ticket.

The most notable European game was a UEFA Cup tie with Bayern Munich, which saw City hold the Germans 1:1 at Musgrave Park before falling 0:2 to late goals in Bavaria.

Damien Richardson took the helm and the 1993/94 season began with City coming from three goals down to beat Welsh side Cwmbran Town in the UEFA Champions League.

After a strong start to the season, financial pressures forced Richardson to resign and with Bishopstown not being developed to plan, games were switched to Cobh, Turners Cross, and an enforced trip to Tolka Park.

Cork began the following season with eight straight wins but in the end had to settle for second place, as three defeats to champions St Patrick's Athletic were costly.

Dolan's second season as manager also proved successful, as City surpassed Malmö FF and NEC Nijmegen in the Intertoto Cup and secured second place in the league.

2006 saw further upgrade work begin at Turners Cross and City met Apollon Limassol and Red Star Belgrade in the UEFA Champions League.

This mirrored an inconsistent season start, with elimination from the Setanta Cup, a home win against St. Pat's and a record-equaling 4–1 defeat to Sligo Rovers.

Paul Doolin replaced Mathews as manager for the 2009 season,[18] and the side gained a number of positive results early in 2009 – including defeating Roy Keane's touring Ipswich Town 2–0.

[19] Despite these on pitch results however, the club's future was left in considerable doubt following a High Court decision on outstanding Revenue receipts.

[28] Mounting pressure on owner Tom Coughlan (including threatened boycotts[29] and censure by the FAI)[30][31] resulted in his resignation as chairman.

The name of the club was restored on 1 June 2010 when a supporters' trust, FORAS, completed the purchase of the rights from Cork City Investments FC Ltd's liquidator.

[43] The club were knocked-out of the 2012 FAI Cup by Shamrock Rovers in the third round, and finished sixth in the 2012 Premier Division league competition.

Former veteran player and record scorer John Caulfield was appointed manager in 2014, and oversaw unbeaten runs at the start[46] and end of the season – keeping pressure on league-leaders Dundalk.

[47] However, despite pushing the title to a final day decider, Caulfield's side failed to pick up points from Dundalk and finished second in the 2014 Premier Division competition.

However, in November they beat Dundalk in the 2016 FAI Cup final after Sean Maguire scored a last minute extra time goal to win Caulfield his first major trophy as manager.

[55] City started 2018 with a third successive President's Cup final win over Dundalk - in a game overshadowed by the death of former player Liam Miller, who died earlier in February 2018.

[59] Neale Fenn was appointed as Caulfield's replacement in August 2019,[60] following a period where Frank Kelleher and John Cotter held interim management and coaching positions.

[64] The club's relegation to the League of Ireland First Division was sealed on 24 October 2020, as their bottom of the table 10th-place finish was confirmed following a Finn Harps win over Bohemians.

[65] In late October 2020, the supporters' trust agreed to sell the club to Preston North End owner Trevor Hemmings through his company Grovemoor Limited.

[66] However, in mid-December 2020, it was reported that the proposed sale would not progress, as Grovemoor Limited could not agree "terms on a lease agreement with the Munster Football Association" for the use of Turner's Cross.

[72] In November 2023, after finishing ninth and losing to an extra-time penalty in the 2023 playoff decider,[73] Cork City were again relegated to the LOI First Division for the 2024 season.

[75] A "youthful" and "experiment[al]" Cork City side were knocked out of the 2023-2024 Munster Senior Cup by Wilton United at the last-16 stage.

[77] With six games to spare and after a 12-game unbeaten run, Cork City secured the First Division title and automatic promotion after a win against UCD in early September 2024.

Since the club's inception in 1984, the kits also featured a red trim – influenced in part by the traditional Gaelic Athletic Association (GAA) colours of County Cork.

[94] In 2004, a Cork XI selection featuring a number of City players faced Bolton Wanderers, wearing yellow and black.

[6] "The Shed" is a section of seating in the Curragh Road stand which is home to Cork City's more vocal supporters and ultras group "Commandos 84".

Commandos 84 were formed in 2004 with the aim of adding organised displays, noise and colour to the Shed with drums, flags, banners and pyrotechnics.

[110] Following a game in May 2023, "disgusting" chants (which referred to his young son with leukemia) were directed from outside Cork City's ground at Shamrock Rovers' manager Stephen Bradley.

[111][112] The incident was condemned by local businesses and the club,[113] and Bradley subsequently thanked the "genuine fans of Cork City" for their support.