He has been moderately successful as a football player and as a coach, which included two stints with the Dutch national football team. He has coached a number of clubs in the Netherlands and abroad (including the Russian club FC Zenit Saint Petersburg, with whom he won the 2008 UEFA Cup Final), as well as the national teams of a number of other countries, including South Korea, the United Arab Emirates, and Belgium. His nickname is "The Little General", a reference to his mentor Rinus Michels' sobriquet "The General."

Advocaat was a defensive midfielder during his playing days. His career began as an 18-year-old with Hague club ADO Den Haag, and he made his debut with the club as 21-year old in 1967. His professional debut was 21 May 1967 in a 3–0 win against GVAV. He only featured for Den Haag once more that season, and that summer the San Francisco Golden Gate Gales franchise imported the Den Haag team, which included Advocaat, to play for six weeks in the United Soccer Association as part of an effort to make the sport more popular in the country. It was the following season that Advocaat won his only honour as a player, the Dutch Cup in 1968. In the 1969–70 he became a regular in the team, making 29 appearances that season and scoring his first goal for the club; he made 33 appearances the season after that. From the 1971–72, the club merged with Holland Sport and became FC Den Haag. In that season and his final season, Advocaat made a further 66 appearances and scored 6 goals. In total he made 147 appearances and scored 7 goals for the club.

From 1973, his playing career continued for Roda JC until he moved to VVV-Venlo during the 1976–77 season. In his time at Roda JC, Advocaat made 121 appearances and scored 2 goals, and when the club was to be discontinued in 2009, Goal.com described him as their most famous player. In his first season with VVV-Venlo, Advocaat scored 2 goals in 20 appearances. He made 33 appearances in the 1977–78 season, scoring 4 goals, and made a further 21 appearances in his final season at the club. In total, he made 74 appearances and scored 6 goals.

In 1978, Advocaat made the move to America to play with Chicago Sting in the North American Soccer League (NASL). That season he made 24 appearances, scoring 2 goals. In 1979 he scored 3 more goals in 28 appearances and for the 1980 season he scored 1 further goal from 29 appearances. During the break between the 1979 and 1980 NASL seasons, Advocaat returned to the Netherlands and made 11 appearances, scoring 1 goal, for his former club FC Den Haag.

Following the 1980 NASL season, Advocaat moved to Sparta Rotterdam to play the remainder of the 1980–81 season. He spent eighteen months at the club scoring 6 goals and making 61 appearances. Following that Advocaat moved to Belgium and played in the second division for K. Berchem Sport, however he only made 10 appearances before, moving back to the Dutch Eredivisie with FC Utrecht where he made 39 more appearances before the end of his playing career.

As well as playing football Advocaat was a PE teacher and became involved in coaching in 1981 (aged 32) when his older brother, Jaap, was offered a job running amateur Saturday football side Door Samenwerking Verkregen Pijnacker (DSVP). Jaap did not take the role but recommended Dick for the job. Advocaat coached this side during the final four years of his playing career with Sparta Rotterdam and Utrecht.

In 1984, Advocaat was unexpectedly appointed as assistant to Dutch national team coach Rinus Michels. Advocaat became a protégé of Michels, who's sobriquet was "The General". In reference to this, Advocaat acquired the nickname "The Little General". In 1987, Advocaat became manager of his first professional club, HFC Haarlem. He stayed at Haarlem for two years before moving to Schiedamse Voetbal Vereniging (SVV) as manager. At SVV, alongside technical director Wim Jansen, Advocaat led the team to become Eerste Divisie champions in the 1989–90 season winning promotion to the Eredivisie. In 1991, SVV merged with neighbouring club Dordrecht '90, who failed to win promotion to the 1990–91 play-offs. SVV had finished 16th the previous season, but remained in the Eredivisie after winning their relegation play-off. The two teams competed as SVV/Dordrecht '90 during the 1991–92 season and became FC Dordrecht the following season, after Advocaat had left. Despite success at both clubs, Advocaat was criticised in his initial coaching years for playing defensive football.

In 1990, Advocaat once more became an assistant to Michels, who was having his fourth spell as coach of the Dutch national team and looking to qualify for Euro 1992. During UEFA Euro 1992, it became apparent it would be Michels' last job and following the tournament Advocaat took over as national coach. Advocaat lost his first two matches in charge, a friendly against Italy and a World Cup qualifier against Norway. During the qualifying campaign Advocaat and Ruud Gullit fell out; Gullit was unhappy with Advocaat's tactics in the World Cup qualifier against England and was eventually substituted. Following this Gullit retired from international football, but was widely expected to return with a change of administration in the summer. Advocaat qualified for the World Cup, following a crucial win against qualification rivals England. Despite the result, Advocaat was scheduled to lose his job to Johan Cruyff for the 1994 FIFA World Cup. However, talks between Cruyff and the KNVB broke down at the last minute and Advocaat retained his position, causing Gullit to remain in retirement. At the World Cup, Advocaat led the Dutch to the quarter-finals where they lost 3–2 to eventual winners Brazil. Following the World Cup, Advocaat returned to manage at club level.

Advocaat returned to coaching at club level with PSV Eindhoven in 1995, taking over from interim manager Kees Rijvers; PSV finished third that season. Coming to the club, Advocaat coached existing players Ronaldo and Luc Nilis, and in 1995–96, Advocaat's first full season with the club, he led PSV to second place in the Eredivisie. They also won that years KNVB Cup which qualified them for the following years UEFA Cup Winners' Cup. Over the summer Advocaat signed Jaap Stam, and in the 1996–97 season PSV won the Eredivisie and qualified for the UEFA Champions League the following year. In June 1998, Advocaat left the club.

In 1998 Advocaat accepted the invitation from Rangers chairman David Murray to become the Scottish Premier League team's new manager. This was despite Walter Smith still being in the job. Shortly after joining Rangers Advocaat fronted a notable advertising campaign for Hair transplantation.