Flora is often regarded to be the flagship of Estonian football due to the club policy of promoting young Estonian players through the ranks and several managers having coached both Flora and the Estonia national football team at the same time in the past.
After the first season, the league was reformed to run from autumn to spring, as most of the European top-level football leagues do. Flora finished the 1992–93 season as runner-ups with 34 points behind Norma, who claimed their second league title with 42 points.
In January 1996, Teitur Þórðarson replaced Ubakivi as a manager. Disappointing start in the 1995–96 Meistriliiga left the team in second place behind Lantana. Lembit Rajala won the goal scoring title with 16 goals. Flora finished the next season in second place behind Lantana once again. Mart Poom broke the club record by keeping a clean sheet for 756 minutes. Flora won their first league title under Þórðarson in the 1997–98 Meistriliiga season. After the season Meistriliiga format was reformed once again and the club managed win another title in the same calendar year. Flora also competed in the UEFA Champions League for the first time in 1998, narrowly losing to Steaua București 4–5 on aggregate in the first qualifying round.The club added another Estonian Cup trophy after defeating Lantana 3–2 in Kuressaare. Flora also met Italian Milan in a friendly match, ending in a 1–2 defeat. Since 1999, Meistriliiga adopted the current league format with the season running from spring to autumn within a single calendar year. In Andres Oper, the club's top goalscorer in three previous seasons, left the team in July. The 1999 Meistriliiga was unsuccessful; Flora placed third, while Levadia won the title and Tulevik came in second. In 2000, Tarmo Rüütli was hired as the new manager. Under Rüütli, Flora finished the 2000 Meistriliiga season second, behind Levadia, who won the title without a single loss during the season.
In 2001, a new era began for Flora as the club moved to the new Lilleküla Stadium. Rüütli returned to Tulevik and was replaced as manager by Arno Pijpers. Under Pijpers, Flora won three consecutive Meistriliiga titles in 2001, 2002 and 2003. In 2003, Flora won the league without losing a single match and from 2002–03, the team went unbeaten in the Meistriliiga for 37 matches. In 2003, Tor Henning Hamre also broke the club goal scoring record by 39 goals. Pijpers left Flora in September 2004, before the end of the 2004 season and was replaced by Janno Kivisild. The team failed to defend the title for another season, finising in third place. Vjatšeslav Zahovaiko won the goal scoring title with 28 goals.
The 2005 season was unsuccessful as Flora placed fourth, 26 points behind the league champions TVMK. This was the first time Flora didn't win a Meistriliiga medal since 1992. After the disappointing season, Kivisild was replaced by Pasi Rautiainen. In the 2006–07 UEFA Cupqualifying rounds, Flora defeated Lyn Oslo 1–1 on aggregate on away goals in the first qualifying round, before losing to Brøndby 0–4 on aggregate in the second qualifying round. The club finished the 2006 Meistriliiga season in third place and came second in 2007. In 2007, Flora also suffered their biggest margin of defeat in the Meistriliiga thus far, losing 0–6 to TVMK. Flora finished the 2008 season second behind Levadia once again, despite 91 points and 113 goals scored. In 2009, Tarmo Rüütli returned to Flora, replacing Rautiainen as manager but failed to guide the club to winning the league, placing fourth. The club was more successful in the Estonian Cup, winning the trophy in 2008 and 2009.
In 2010, Rüütli was replaced as manager by the former Flora player and Estonia national football team record cap holder Martin Reim. Under Reim, rejuvenated Flora ended the reign of Levadia who had won the four previous Meistriliiga titles by winning the 2010 season, while Sander Post won the goal scoring title with 24 goals. Flora successfully defended their title in 2011 and won the 2010–11 Estonian Cup, defeating Narva Trans 2–0 in the final. Flora finished the 2012 Meistriliiga season in third place, behind the winners Nõmme Kalju and Levadia. Reim left the club and Marko Lelov was hired as the new manager. Lelov won the 2012–13 Estonian Cup in April but was sacked on 20 July after disappointing results in the Meistriliiga. He was replaced by Norbert Hurt, initially as a caretaker manager with position being made permanent later. Flora finished the 2013 season in fourth place and placed third in 2014. In 2015, Flora celebrated their 25th anniversary as a club by winning their 10th Meistriliiga title in the 34th round of the season.