Dinamo Minsk is a club whose greatest achievement came at a time when it was the only representative of its republic in the top flight of Soviet football. Its birthday is counted from 18 June 1927, when a team of the Dinamo sports society in the Byelorussian republic beat a side from Smolensk 2–1 in a friendly. The club spent part of its early history in the lower divisions, and in 1940 it was promoted to the Soviet Top League, becoming the first and, for the whole Soviet period, the only Belarusian team to play at that level. Over the years it spent 39 of 54 seasons in the top division, and in the Byelorussian Cup of the Soviet era it won the trophy in 1936 and 1940. The white and blue colours earned it the nickname of "the white-blues".
The golden season came in 1982, when Dinamo Minsk won the Soviet championship, the first and only such title for a Belarusian club. Under coach Eduard Malofeev the team finished the 34-match season with 19 wins, 9 draws and 6 defeats, scoring 63 goals and collecting 47 points. Dynamo Kyiv finished second with 46 points, only a single point behind. The two met in Minsk on 27 October 1982, when the Dinamo Stadium was reportedly filled with some 50,000 spectators for a match that ended 1–1. Minsk had effectively taken the first place in the table, while Kyiv also took a medal. The title was not a one-off, because the team finished third in the following season.
The championship brought a European debut in the 1983–84 European Cup, and Dinamo Minsk reached the quarter-finals. There it was eliminated by Dinamo Bucharest, who were themselves stopped in the semi-final by the eventual winners, Liverpool. It remains the club's best result in Europe. Over the years the team added two appearances in the Cup Winners' Cup after reaching the final of the Soviet Cup, which shows how consistently it competed at the top level in the last decade of the Soviet Union.
After the collapse of the Soviet Union, Dinamo Minsk dominated the first years of independent Belarusian football. The club won the first five Belarusian championships in a row and has seven league titles in total: 1992, 1992/93, 1993/94, 1994/95, 1995, 1997 and 2004. It also won the Belarusian Cup three times, in 1992, 1993/94 and 2002/03. In 1993 it made its only appearance in the UEFA Champions League. After the early dominance, the club was overtaken in the national table by BATE Borisov, which won most of the titles that followed. It had its own European moment in 2014–15 and again in 2015–16, when it reached the group stage of the Europa League, becoming the second Belarusian club to do so after BATE.
The team plays its home matches at the Dinamo National Olympic Stadium in the centre of Minsk. The ground opened in 1934 and was rebuilt in preparation for the 1980 Olympic Games in Moscow, for which Minsk hosted part of the football tournament, and it was later modernised again. In recent years the club has again been among the leading sides of the Belarusian league, and it finished second in 2025. The memory of the Soviet title nevertheless remains the central point of its identity. In a country where few clubs have comparable history, Dinamo Minsk is the one that proved that a team from Belarus could win the championship of the Soviet Union.