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FC Pirin

One of FC Pirin Blagoevgrad's predecessors, FC Pirin, was founded in 1922. FC Pirin has played more than 20 seasons in the top flight and has competed twice in the European football competitions with one participation in the UEFA Cup and one participation in the Cup Winners' Cup respectively. The club's first participation in the UEFA tournaments was not promising. In 1985, Pirin faced the then reigning Swedish champion Hammarby IF. The first game in Blagoevgrad, ended with a 1–3 loss. The second game in Sweden was also a defeat – 0–4 and Pirin were out of the European competitions. Pirin's best season in the Bulgarian top division was in the 1984–85 season, where they finished at 5th place at the end of the season. The club was also three times runner-up of the Bulgarian Cup. Also, Pirin's youth academy is attributed as being one of the best developers of young and unknown players in Bulgaria. Among the club's famous players are Dimitar Berbatov, Spas Delev, Petar Mihtarski, Ivaylo Andonov, Ivan Tsvetkov, Vladislav Zlatinov and Petar Zlatinov.

On August 18, 2006, after failing to arrange some debts and signals of corruption, Pirin was expelled from the A PFG, the team's results for the season were annulled, and the club was relegated to the Bulgarian South-West V AFG. However, after two years, Pirin won the South-West V AFG and the club returned for the upcoming season of the Western B PFG.

Unification

In December 2008, Pirin, which competed in the Western B PFG, was merged with PFC Pirin Blagoevgrad, (former FC Makedonska Slava), which played in the A PFG after a significant pressure from the supporters in the town. The new club was named FC Pirin Blagoevgrad and was soon proclaimed as a holder of the club records of the former FC Pirin, which competed for more than 20 seasons in the top flight. FC Pirin's West B PFG place was taken by FC Bansko. Then, Nikolay Galchev appointed Petar Mihtarski as a manager of the club. A few months later, under Naci Şensoy's management, the successes followed-up and Pirin qualified for the final of the Bulgarian Cup, eliminating subsequently on their way CSKA Sofia and Levski Sofia. In the final match played at the Georgi Asparuhov Stadium in Sofia, Pirin were eliminated after a 3–0 defeat against Litex Lovech.

OFK Pirin

In the foremath of the 2011–12 season, Pirin Blagoevgrad failed to receive a professional license for the A Group. However, due to their financial struggles they were also rejected to participate in the South-West V AFG. Later that year, they acquired the license of Perun Kresna. The team finished 2011-12 season as Perun, but for 2012-13 the team was renamed to Obshtinski futbolen klub Pirin (Bulgarian: Общиснки футболен клуб „Пирин“), meaning Pirin Minicipal Football Club, as the club was owned by Blagoevgrad Municipality.

In 2015, the club achieved promotion to the A Group after a four-year absence from top-flight football. The 2015-16 season ended in an 8th place finish out of 10 teams in a modified season format. The next season (2016–17), Pirin again managed to avoid relegation. However the team was relegated from the A Group after the 2017-18 season.

On 11 June 2019, OFK Pirin secured a one-year sponsorship agreement and advertising partnership with the investment company Emirates Wealth EAD. In July, Blagoevgrad Municipality approved a business plan by the company discussing the future development of the club, in particular the partnership between the two sides, phases in acquiring participatory management, investment schemes, club finances and aims. The plan saw Emirates Wealth EAD become a majority owner, as it acquired 75% of the OFK Pirin's shares, with 25% remaining in Blagoevgrad Municipality's ownership. Part of obtaining participatory management saw the creation of a new association, a joint-stock company named Futbolen klub Pirin AD (Bulgarian: Футболен клуб „Пирин“ АД), meaning Pirin Football Club, where OFK Pirin, owned by the municipality, was merged into.

In 2021, Pirin managed to return to the First League after three years of absence.