Gullit was born Ruud Dil in Amsterdam to George Gullit, an Afro-Surinamese migrant, and Ria Dil, his buitenvrouw, from the Amsterdam Jordaan inner city district. The family lived in one split level room on the top floor of a small apartment building. Gullit's father worked as an economics teacher at a local school, his mother as a custodian at the Rijksmuseum.

Gullit developed his football skills in the confines of the Rozendwarsstraat, and street football was instrumental in his formative years. Gullit's first team were the Meerboys, where he joined as a junior in 1970. However, at the age of 10 Gullit moved from the Jordaan to Amsterdam Old West where he played street football alongside Frank Rijkaard. Gullit joined the DWS club after his move, and came to the attention of the Dutch youth team, where he played alongside such future greats as Erwin Koeman, Ronald Koeman and Wim Kieft.

It was during his time at DWS that Ruud first took to using his father's surname, rather than his registered surname, as he thought it sounded more like a football player. He retained his mother's surname, officially, and continues to sign all contracts as Ruud Dil.

In 1978, he signed professionally for HFC Haarlem under coach and former West Bromwich Albion F.C. player Barry Hughes. Gullit made 91 league appearances for Haarlem, scoring 32 goals. Gullit made his debut for the club at just 16 years old, becoming at the time the youngest player in the history of the Eredivisie. In his first year at Haarlem they finished bottom of the Eredivisie, but bounced back the following season winning the Eerste Divisie. Gullit was named as the best player in the Eerste Divisie that season. in recognition of his outstanding efforts. In the 1981–2 season Gullit was in fine form as Haarlem finished 4th and qualified for Europe for the only time in their history. In that same season Gullit scored the goal he would later consider his finest, "Playing against Utrecht I went past four defenders and then the goalkeeper, and scored. It was an unforgettable goal for me." Hughes was so impressed with the young Gullit that he described him as the "Dutch Duncan Edwards".

In 1982, he moved to Feyenoord, for a fee of £300,000, where he made 85 league appearances, scoring 31 goals. At Feyenoord Gullit found himself playing alongside Dutch legend Johan Cruijff, while the assistant manager was Wim van Hanegem, and they were to leave a lasting impression. Gullit's first season saw Feyenoord miss out on major honours, but the following year they completed the league and cup double. Gullit was named Dutch Footballer of the Year in recognition of his contribution to Feyenoord's success. At Feyenoord Gullit occupied an increasingly advanced role in midfield, having played predominantly as a sweeper at Haarlem. While at Feyenoord Gullit became the focus of a race row as manager Thijs Libregts was alleged to have referred to Gullit as "blackie" and criticised him for being lazy, though Libregts defended himself by claiming that it was merely a nickname. While playing for Feyenoord at St Mirren in September 1983 he was racially abused and spat on by Scottish supporters. Gullit called it "the saddest night of my life".

In 1985, he moved to PSV for ƒ1.2 million (£400,000), and wound up scoring 46 goals in 68 league appearances for the team. Gullit was again named Footballer of the Year in 1986 as he helped PSV capture the Eredivisie crown, a feat they repeated the following year. It was at PSV that Gullit really began to establish himself as a world class footballer and his distinctive, dreadlocked appearance made certain that he would catch the eye of Europe's biggest clubs. Gullit was also singled out for criticism by large numbers of Feyenoord supporters, who branded him a "wolf" and accused him of moving to Eindhoven for money.

Silvio Berlusconi signed Gullit for AC Milan in 1987, paying the then world record transfer fee of ƒ18 million (£6 million) as a replacement for Ray Wilkins. Among his teammates at that club were compatriots Marco van Basten and Frank Rijkaard, along with Paolo Maldini and Franco Baresi. Gullit's exploits with first PSV and then Milan helped him win the European Footballer of the Year award in 1987 which he dedicated to Nelson Mandela.

When he arrived at Milan, Gullit initially struggled to settle as he spoke no Italian and was unused to living in a foreign country. However, Gullit's first season at Milan saw the club win Scudetto for the first time in 9 years, under coach Arrigo Sacchi. He was initially used on the right of an attacking trio alongside Van Basten and Pietro Virdis, but after an injury to Van Basten it was changed to a front two. The following season Milan built on their domestic success by adding the European Cup to their list of honours. Their scintillating 5–0 demolition of Real Madrid in the semi-final second leg came at a cost, as Gullit suffered an injury and required surgery to be fit in time for the final. That performance was followed by a 4–0 victory over Steaua Bucharest in the 1989 final with Gullit scoring two crucial goals. The following year Milan retained the trophy as they defeated Benfica in the 1990 final. However, serious injuries sustained to the ligaments of his right knee limited Gullit's playing time and he managed just 2 domestic games in the 1989–90 season before appearing in the cup final.

In 1990–91 Milan's pursuit of a third consecutive European Cup was cut short by Olympique de Marseille at the semi-final stage. Having drawn the first leg at the San Siro, Milan trailed to a Chris Waddle goal with little time remaining when the floodlights went out. After a short delay the lighting was restored, but Milan had returned to their dressing room and refused to return to complete the game. UEFA awarded Marseille a 3–0 victory and expelled Milan from all European competitions for the following season.

While Milan continued their domestic dominance by winning Serie A in both 1991–92 (a season in which they went undefeated) and 1992–93, Gullit's position was an increasingly peripheral one. This was demonstrated by his omission from the UEFA Champions League Final 1993 final as under the UEFA rules clubs were only allowed to field 3 foreigners.