In 1981, on his 19th birthday, Gullit made his international debut as a substitute for the Netherlands national team against Switzerland, a game the Dutch lost 2-1.

Gullit's early international career was marred by disappointment as the Dutch failed to qualify for the 1982 FIFA World Cup and Euro 84. The Dutch missed out in 1984 on goals scored as the Spanish trounced minnows Malta 12-1 in their final qualifying game, when they needed an 11 goal victory to qualify.

There was further disappointment in 1986 when the Dutch missed out on qualification for the World Cup at the hands of neighbours Belgium in a play-off. Having lost 1-0 in Belgium, the Dutch appeared to be set for qualification in Rotterdam as they led 2-0 until Georges Grun put the Belgians through on away goals.

However, Gullit was one of the key players for the Netherlands helping his country win the Euro 88 under coach Rinus Michels. Having lost their opening game of the tournament to the USSR the Dutch beat England and Republic of Ireland to reach the semi-finals. After defeating West Germany 2-1 in Hamburg the Dutch faced the Soviet Union in the final. Gullit opened the scoring with a well-placed header and Marco van Basten scored an incredible volley to cap a 2-0 win. Ruud Gullit was thus the first Dutch captain to hold aloft international silverware.

The Dutch travelled to Italia 90 as one of the favourites, but the team failed to perform as expected. Gullit's knee injuries clearly hampered his play, and his only moment of brilliance was a superb dribble and shot against Ireland which helped the Netherlands qualify for the second round. There they met W Germany in one of the most exciting games of the tournament, though the game was marred by an altercation between Frank Rijkaard and Rudi Voller. The Germans gained revenge for their defeat at Euro 88, by beating the Netherlands 2-1 and going on to win the tournament.

1992 saw the Dutch again among the favourites for silverware in Sweden at Euro 92. Gullit appeared in imperious form against Scotland in their opening game of the tournament as he supplied Dennis Bergkamp with an easy goal. But after drawing with Russia and beating Germany, the Dutch suffered a shock exit on penalties to Denmark, who ended up winning the championship's Henri Delaunay Trophy.

In 1993 Gullit and Holland manager Dick Advocaat began what was to be a long running dispute which ultimately ended Gullit's international career. Advocaat's decision to play Gullit on the right-side of midfield, in a game against England at Wembley, rather than his usual central position upset Gullit and this was exacerbated by his substitution for Marc Overmars. Gullit refused to play for the national team following this but later changed his mind and agreed to return, facing Scotland in May 1994. Shortly before the 1994 FIFA World Cup, Gullit walked out of pre-tournament training camp and would never play international football again.