After being rejected on two previous occasions by the club, Davids started his career at the age of 12 with Ajax. He made his first team debut on 6 September 1991 in a 5–1 home win over RKC Waalwijk. He helped the Amsterdam club to three domestic Eredivisie titles, as well as continental success with the 1992 UEFA Cup and the 1995 UEFA Champions League. In the 1996 UEFA Champions League final, he missed Ajax’s first penalty in the shoot-out, which they ultimately lost to Juventus. While at Ajax, Davids was nicknamed “The Pitbull” by Ajax manager Louis van Gaal due to his fierce style of play in the team’s midfield.

Davids was an integral part of the Netherlands national team since his debut on 20 April 1994 in Tilburg against the Republic of Ireland (0–1), though he has not won any major tournaments for the Oranje.

Davids has appeared in commercials for the American sportswear company Nike. In 1996, he starred in a Nike commercial titled “Good vs Evil” in a gladiatorial game set in a Roman amphitheatre. Appearing alongside football players from around the world, including Ronaldo, Paolo Maldini, Eric Cantona, Patrick Kluivert and Jorge Campos, they defend “the beautiful game” against a team of demonic warriors, before it culminates with Cantona striking the ball and destroying evil.

At the start of the 1996–97 season, Davids moved to Italy to play for Milan. After an unsuccessful spell where he failed to establish himself in the first team, he moved on to league rivals Juventus in December 1997 for a £5.3 million transfer fee. He soon became a permanent first team member in the midfield, usually playing on the left flank or in the centre, as a defensive midfielder, forming a notable midfield partnership alongside French playmaker Zinedine Zidane. Six successful years in Turin followed, with Davids helping the side to the Serie A title in 1998, 2002 and 2003, as well as two Supercoppa Italiana and the UEFA Intertoto Cup. Juventus manager Marcello Lippi once described him as “my one-man engine room”.

Davids was often inspirational in Europe, playing 15 times as the club made it all the way to the 2002–03 Champions League final before losing to Milan on penalties. He had also previously managed to reach the Champions League final with Juventus in 1998, followed by a semi-final finish during the 1998–99 season, as well as reaching the 2002 Coppa Italia Final.

In 1999, Davids began wearing protective glasses following surgery in his right eye caused by glaucoma, which developed in 1995 following eye injuries. Davids first wore them on 4 September 1999 in a friendly match against Belgium. On 17 May 2001, Davids was suspended by FIFA when he tested positive for the banned anabolic steroid, nandrolone.

Davids was engaged to fashion designer Olcay Gulsen. In 1999, Davids started his own Street Soccer fashion label called Monta Soccer. It offers urban style clothes for men, women, and children around the world. It currently has multiple fashion lines. The Monta Sports, The Monta Studio and Monta Juniors.

Davids joined Barcelona on loan in January 2004 from Juventus. Joining midway through a season where the club was struggling in mid-table and recently appointed manager Frank Rijkaard was under considerable pressure, Davids led Barça’s successful resurgence of form which saw them finishing second to Valencia in La Liga. Davids’ arrival has been cited as the catalyst for the Catalan club’s dominance of Spanish and European football during the mid-to-late 2000s (decade), with Barcelona winning La Liga the following season (after five years without winning the league title) and a La Liga and Champions League double in 2005–06.

After Euro 2004, new national team coach Marco van Basten appointed Davids as captain of the team. However, lack of first team football at his club Inter meant Davids also lost his place in the national team in October 2004, thus losing the captain’s armband in the process, which was later handed to goalkeeper Edwin van der Sar. At the latter stages of the qualifying series for the 2006 World Cup in October 2005, he was recalled back into the national team, though not as captain. He fell out of the picture again shortly after, thereby missing out on the Dutch squad for the World Cup.

In the summer of 2004, Davids permanently moved on to Italian club Inter Milan on a three-year contract. When Inter terminated the remaining years of his contract in August 2005, he moved to England on a free transfer to play for Tottenham Hotspur. He had a successful stay at Tottenham and instantly became a fan favourite. His first and only goal was in a 2–1 away win against Wigan Athletic. Davids played for Spurs in the 2005–06 and the 2006–07 seasons, with the club finishing fifth in both seasons.

Davids signed once more for Ajax on 28 January 2007 and played his first match against club rivals Feyenoord on 4 February. After the mid-season switch, Davids proved his value for the Ajax team again. He was one of the key midfielders in the run for the Dutch championship that was lost on one single goal to PSV on the final day of the league. He also played a major role in Ajax’s cup campaign. He secured the KNVB Cup for Ajax by scoring the final penalty in a thrilling penalty shoot-out against AZ. Prior to the start of the 2007–08 season, Davids’ leg was broken in a pre-season friendly against Go Ahead Eagles, sidelining him for around three months. In May 2008, Davids said he would leave Ajax when his contract expired on 30 June.

Davids played against the LA Galaxy on 6 December 2008 in an exhibition match held at Mount Smart Stadium in Auckland, New Zealand, as part of an Oceania XI All-Star team, despite the fact he is not from Oceania and has never played for an Oceanic club or national team. Davids was in contract negotiations with English Championship club Leicester City from 22 October 2009, however he failed to make a decision for over a week and the club withdrew their offer on 30 October.

On 20 August 2010, Davids agreed a pay-as-you-play deal with English Championship club Crystal Palace. He made his debut on 24 August 2010 at left-back in the Second Round of the League Cup against Portsmouth. On 8 November 2010, he announced his departure from the club, stating it was “one of the greatest experiences of my life”.

Since 2010, Davids had been living in North London with his partner and had been participating in street football as well as managing Sunday league amateur side Brixton United. On 11 October 2012, Davids joined League Two side Barnet in a player-manager role, alongside Mark Robson. The next day, on his managerial debut for Barnet, his side lost 4–1 at Underhill to Plymouth Argyle which Davids had left himself out of the squad for this League Two game. They followed this up with a 4–0 home win over Northampton Town where Davids played the full match, captaining the team and being voted Man of the Match. In November, he started against Morecambe which Barnet lost 4–1. Near the end of December 2012, following the departure of Robson, Davids took charge of the club by himself. Davids scored his first goal for Barnet in February 2013 in a 2–0 home victory over Southend United.

In June 2011, Davids was elected to the new supervisory board at Ajax alongside Johan Cruyff.

Having seemingly retired from football, Davids was living quietly in North London, when League Two-side, Barnet, approached him with a view to becoming joint player-coach alongside Mark Robson. In December 2012, Davids was appointed sole player-manager. During his time there he was famous for certain quirks and controversies. Giving himself the squad number of 1 was almost certainly a unique occurrence for an outfield player-manager, as was a refusal to travel to any away games that required an overnight stay. In 2012-13 season, Davids played almost 30 times for Barnet as they struggled to avoid the drop back into non-league football. That they were ultimately unsuccessful and lost their league status on the last day of the season. The move into Conference Premier football did not go smoothly. Bookings in each of his first eight matches at this level were accompanied by three sending offs, and in January 2014 Davids finally called time on his spell at Barnet. One particular memory that probably shines brightly for Barnet supporters, however, is the time he ordered the team bus to pick up a group of supporters whose transport had broken down on the way home from a defeat at Accrington Stanley.

In March 2013, on the return journey from a defeat at Accrington Stanley, Davids sent the Barnet team coach back to pick up 36 supporters whose coach had broken down on the motorway and take them to the next service station.

Despite initially guiding Barnet off the foot of League Two, and lifting them out of the relegation zone, Barnet dropped back into the bottom two on the final day of the 2012–13 season, following a defeat to Northampton Town, and were relegated out of the Football League at the expense of AFC Wimbledon who were able to escape by beating Fleetwood Town. On 21 May 2013, it was announced that Davids would remain in charge of Barnet for the club’s 2013–14 Conference Premier season. In July 2013, Davids announced his decision to wear the number 1 shirt for the 2013–14 season, a shirt number traditionally worn by goalkeepers, saying that he intends to “set a trend” of midfielders wearing the number 1 shirt.

Discipline was a major problem for Davids in the 2013–14 season. He was booked in each of the first eight league games he played, and he was sent off three times in those first eight games. There was also controversy when it emerged that he would not attend away games that required an overnight stay, leaving assistant manager Ulrich Landvreugd to take charge. In December 2013, Davids considered retiring from football after being sent off for the third time in the season in Barnet’s 2–1 defeat by Salisbury City.

Davids resigned from his post as manager on 18 January 2014.

In June 2014, Southern Counties East Football League side Greenwich Borough announced they were “in advanced talks” with Davids, with chairman Perry Skinner stating that he was “70% sure he’ll come on board”. The following month it was announced the club’s attempt to sign Davids had been unsuccessful.

In 2020, Davids was appointed assistant coach of Dutch Eerste Divisie club Telstar.