Being an amateur team for quite a while and playing in regional leagues, the team was promoted three times during the direction of Noel Graet, who assumed the presidency in 1972. In the year 1976, Guingamp reached the Third Division (now known as Championnat National), and in the following season, they were elevated into the Second Division (now called Ligue 2) and continued until 1993. Guingamp officially became professional in 1984. In 1990, the Stade de Roudourou was opened in the year 1990, which saw Guingamp playing Paris Saint-Germain in the inaugural match.
The club's first major achievement is being awarded the Coupe de France in 2009 as the only team in the history of football not belonging to Ligue 1 to win the event. The team beat Breton opponents Rennes by a score of 2-1 during the championship. Also, in 2014, En Avant de Guingamp beat Stade Rennais F.C. 2 to 0 on the Stade de France. In addition to two years of Coupe de France triumph, the club's most notable achievement is winning in 1996 the UEFA Intertoto Cup.
The club has been within the French top flight previously, but has achieved promotion just three times: in 1995 2000, 2003 and 2013. Their longest stint at the highest level was from 2013 and 2019. After the 2012-13 season, the club was moved again to Ligue 2 at the conclusion of the 2018-19 campaign, which ended in 20th position.
In addition to having won not only the Coupe de France, Guingamp is also known as a springboard to famous players like Didier Drogba Florent Malouda Fabrice Abriel as well as Vincent Candela. Managers like Guy Lacombe, Francis Smerecki and Erick Mombaerts have also utilized Guingamp as a springboard in the beginning of their careers as coaches. Guingamp is ruled by Bertrand Desplat. Guingamp's former president Noel Le Graet, is the president of Guingamp's French Football Federation. It has an women's side that play in Division 1 Feminine, and an reserve team that plays in the CFA2.
For the season 2018-19, Guingamp was able to reach Guingamp's Coupe de la ligue final against RC Strasbourg. Guingamp was defeated in the final, losing 4-1 in penalties after the match was deadlocked for 120 minutes of action.
On May 12, 2019, Guingamp were relegated to Ligue 2 ending a six-year tenure within the first division following losing 1-1 to the club's rivals Stade Rennais F.C.