Dinamo Minsk was founded in 1927 as a part of the Soviet Dinamo Sports Society. They spent some of their history in the lower leagues of the Soviet Union, but in 1940, they promoted in the Soviet Top League, becoming the first and only Belarusian team to compete in the Soviet top division. In 1954, they finished a third place, their best performance in the top flight to date, and were dissolved, being re-founded as Spartak Minsk, only to be renamed in Belarus Minsk in 1959, in honor of the Soviet republic in the national championship. However, in 1962, they return to the original name of Dinamo Minsk.
Dinamo Minsk also participated in Belarusian SSR league. Since mid-50s their appearances were only sporadic and they were represented by youth teams in later seasons. They have won the championship 7 times.
Dinamo Minsk won the inaugural season of the Belarusian Premier League in 1992. They become the top team in the new Belarusian championship and won 5 league titles until 1995, making only one appearance in the UEFA Champions League, in 1993. However, after a title in 1997, Dinamo Minsk last won the championship in 2004. The 2000s saw Dinamo Minsk failing to secure any league title in the battle against BATE Borisov, thus finnishing on lower places, mostly second.
In 2014, Dinamo Minsk beat MyPA, CFR Cluj and Nacional to be drawn in Group K of Europa League, along with Italian side Fiorentina, French team Guingamp and Greek side PAOK, becoming the second team, after BATE Borisov, to reach group stages of Europa League. Dinamo finished at the bottom with four points, after a draw with Guingamp and a historical 2–1 victory over Fiorentina.