Born in Hillingdon, Middlesex, Ray started his career with the Sunday League team Senrab that play in Wanstead Flats, East London.

He made his name in the 1970s with boyhood club Chelsea, which he joined as an apprentice, progressing to his first team debut against Norwich City at the age of 17 on 26 October 1973 as a substitute in a 3–0 home league win.

In 1975, following the club's relegation and the departure of many established players, an 18-year-old he was handed the captaincy of Chelsea by new manager Eddie McCreadie, taking it from long-time Blues captain John Hollins. He took to the role well, keeping it for four years. He emerged as Chelsea's key player of that period, leading a team of mainly young players to promotion again in 1976–1977 and, in the next season, consolidation of their place in the First Division. His rapid success, along with his "dark good looks", also saw Wilkins becoming a regular pin-up feature in British teenybopper magazines.

In 1979, after Chelsea were relegated, Ray signed for Manchester United for a fee of £825,000, the highest fee received for a Chelsea player at the time. He scored ten goals in his five years with the Red Devils, including a long-range strike in the 2–2 draw with Brighton & Hove Albion in the 1983 FA Cup Final.

He was voted player of the year by the team's supporters at the end of the 1983–1984 season. His midfield performances drew the attention of A.C. Milan, who made United a £1.5 million offer for the player.

Ray signed with A.C. Milan in summer 1984. He later remarked that the most difficult part of adapting to the Italian game was the focus on fitness – the coaching staff made him work to reduce his body fat levels and Wilkins described the result as being in the best shape of his career. The Italian team was struggling during this period, having suffered relegation in the 1981–82 Serie A season, and he was joined by fellow Englishman Mark Hateley. The only foreign players in the squad, the pair helped the team to victory over rivals Inter Milan in the Milan Derby that October, winning plaudits from Italian press and the club's fans. In his first year there, Wilkins played 28 Serie A games to bring the team to fifth in the league and also won a runner-up medal in the Coppa Italia.

In his final season there (1986–1987), he fell out of the first team structure, following the signing of Roberto Donadoni. Ray played 105 games for Milan between 1984 and 1987. Corriere della Sera eulogised him as a "serious and meticulous professional who was immediately appreciated for his long and precise passes".

He signed for Paris Saint-Germain in the middle of 1987, but this proved to be short-lived: he failed to break into the team ahead of Gabriel Calderón and Safet Sušić so he eagerly took the option to move to Scotland to sign for Rangers for £250,000 that November.

He became an integral part of the team for the rest of the season, making twenty-nine appearances. However, it would be the following season he would truly make his mark at Rangers. Reigning Scottish champions, and Old Firm rivals, Celtic played Rangers on 27 August 1988. With the score tied at 1–1, Wilkins scored a "thunderous volley" from the edge of the penalty box to put Rangers ahead, and his side eventually recorded an emphatic 5–1 win that day over their rivals. Rangers went on to win the league title that season. Despite only playing two seasons for the Glasgow club, he was later inducted into their Hall of Fame.

The longest stint of his late career was at Queens Park Rangers, for whom he was a regular first team player from November 1989 to 1994. Ray left QPR in the summer of 1994 on a free transfer to join Crystal Palace as a player-coach under manager Alan Smith, but only made one appearance due to breaking his left foot on his debut.

He re-joined QPR as player-manager on 15 November 1994, following the exit of Gerry Francis. As player-manager, he appeared in a further 21 games for the club from 1994 to 1996. He left QPR by mutual agreement in September 1996 after the club was bought by media tycoon Chris Wright following their relegation from the FA Premier League.

Ray played for four clubs in the 1996–1997 season. He played one game at Wycombe Wanderers before moving to Hibernian for a 16-game stint. Toward the end of the season he played three times for Millwall in the Second Division and, finally, three Third Division games for Leyton Orient before retiring.

Wilkins scored three goals in 84 games for England, captained the team on ten occasions and played at the 1982 and 1986 World Cups. Ray was called up to play for England for the first time in 1976 by coach Don Revie, then made his debut on 28 May in a 3–2 win over Italy at the U.S.A. Bicentennial Cup Tournament in New York.
He made his 84th and final England appearance in November 1986, against Yugoslavia.

Ray was QPR manager from 1994 to 1996, and managed fellow West London club Fulham in 1997–1998. In March 1999, Ray was appointed Chelsea's first-team coach as interim manager after the sacking of Gianluca Vialli at the start of the 2000–01 season He was sacked from the club on the orders of new manager Claudio Ranieri in November 2000.

When Vialli was hired by First Division club Watford, Ray again assisted him until their dismissal in June 2002. From 2003 to 2005, he assisted former Chelsea player Dennis Wise in his managing of Millwall, but announced his exit when he took exception at Dave Bassett being hired in the coaching staff.

From 2004 Ray was assistant coach to Peter Taylor with the England under-21s until Taylor left in early 2007. Ray was not retained by incoming head coach Stuart Pearce.

In September 2008, he was appointed assistant first team coach to Luiz Felipe Scolari at Chelsea, following Steve Clarke's departure to West Ham United F.C. In February 2009, following Scolari's shock sacking, Ray was appointed as Chelsea's caretaker manager for the Fifth round FA Cup tie with Watford.

On 11 November 2010, it was announced that Ray's contract with Chelsea "would not be renewed" and that he was to leave the club "with immediate effect". On 1 December 2010, Ray reached what he described as a "harmonious conclusion" with Chelsea following his unexpected departure from Stamford Bridge.

Chelsea manager Carlo Ancelotti, who was himself sacked at the end of the 2010–2011 season, wrote about Wilkins, in his autobiographical book The Beautiful Games of an Ordinary Genius: "Ray is one of those select few, always present, noble in spirit, a real blue-blood, Chelsea flows in his veins ... without him we wouldn't have won a thing."

On 30 December 2013, Ray was appointed assistant head coach of Fulham. He and technical director Alan Curbishley were sacked on 17 February 2014 and the season ended with relegation.

On 3 September 2014, Ray was appointed as the new head coach of Jordan. He led Jordan at the 2015 AFC Asian Cup, where they were eliminated in the group-stages for the first time after two losses against Iraq and Japan and a win over Palestine.

On 25 June 2015, Aston Villa manager Tim Sherwood appointed Ray as his assistant manager. On 26 October 2015, he was sacked along with Tim Sherwood and the rest of the coaching team.

In the 1990s Ray was part of the team that contributed to the Football Italia show that aired on Channel 4. He later appeared as a commentator for Sky Sports, particularly on their Champions League coverage. He also worked for Talksport.

Ray was a patron for the charity Cardiac Risk in the Young. In 1993, he was made an MBE.

On 28 March 2018, Wilkins had a cardiac arrest resulting in a fall and was placed into an induced coma at St George's Hospital in Tooting.

Hours after his death, Milan played rivals Inter Milan in the Derby della Madonnina at the San Siro. His former captain Franco Baresi laid a bouquet of flowers next to Wilkins' shirt by the side of the pitch. A section of Milan fans held aloft a banner which read "Ciao Ray: Leggenda Rossonera" (English: "Goodbye Ray: Legend of the Red and Blacks"). During Chelsea's home game against West Ham United on 8 April, fans at Stamford Bridge gave a minute's applause in the eighth minute to pay tribute to Ray. They also held a banner which read "Ray was one those select few, he knew what it meant to be one of us a real blue blood. Chelsea flowed through his veins, may you rest in peace Ray."

A memorial service was held for Wilkins on 1 May at St Luke's Church, Chelsea, attended by many figures who knew him from the world of football.

Born in Hillingdon, Middlesex, Ray started his career with the Sunday League team Senrab that play in Wanstead Flats, East London.

He made his name in the 1970s with boyhood club Chelsea, which he joined as an apprentice, progressing to his first team debut against Norwich City at the age of 17 on 26 October 1973 as a substitute in a 3–0 home league win.

In 1975, following the club's relegation and the departure of many established players, an 18-year-old he was handed the captaincy of Chelsea by new manager Eddie McCreadie, taking it from long-time Blues captain John Hollins. He took to the role well, keeping it for four years. He emerged as Chelsea's key player of that period, leading a team of mainly young players to promotion again in 1976–1977 and, in the next season, consolidation of their place in the First Division. His rapid success, along with his "dark good looks", also saw Wilkins becoming a regular pin-up feature in British teenybopper magazines.

In 1979, after Chelsea were relegated, Ray signed for Manchester United for a fee of £825,000, the highest fee received for a Chelsea player at the time. He scored ten goals in his five years with the Red Devils, including a long-range strike in the 2–2 draw with Brighton & Hove Albion in the 1983 FA Cup Final.

He was voted player of the year by the team's supporters at the end of the 1983–1984 season. His midfield performances drew the attention of A.C. Milan, who made United a £1.5 million offer for the player.

Ray signed with A.C. Milan in summer 1984. He later remarked that the most difficult part of adapting to the Italian game was the focus on fitness – the coaching staff made him work to reduce his body fat levels and Wilkins described the result as being in the best shape of his career. The Italian team was struggling during this period, having suffered relegation in the 1981–82 Serie A season, and he was joined by fellow Englishman Mark Hateley. The only foreign players in the squad, the pair helped the team to victory over rivals Inter Milan in the Milan Derby that October, winning plaudits from Italian press and the club's fans. In his first year there, Wilkins played 28 Serie A games to bring the team to fifth in the league and also won a runner-up medal in the Coppa Italia.

In his final season there (1986–1987), he fell out of the first team structure, following the signing of Roberto Donadoni. Ray played 105 games for Milan between 1984 and 1987. Corriere della Sera eulogised him as a "serious and meticulous professional who was immediately appreciated for his long and precise passes".

He signed for Paris Saint-Germain in the middle of 1987, but this proved to be short-lived: he failed to break into the team ahead of Gabriel Calderón and Safet Sušić so he eagerly took the option to move to Scotland to sign for Rangers for £250,000 that November.

He became an integral part of the team for the rest of the season, making twenty-nine appearances. However, it would be the following season he would truly make his mark at Rangers. Reigning Scottish champions, and Old Firm rivals, Celtic played Rangers on 27 August 1988. With the score tied at 1–1, Wilkins scored a "thunderous volley" from the edge of the penalty box to put Rangers ahead, and his side eventually recorded an emphatic 5–1 win that day over their rivals. Rangers went on to win the league title that season. Despite only playing two seasons for the Glasgow club, he was later inducted into their Hall of Fame.

The longest stint of his late career was at Queens Park Rangers, for whom he was a regular first team player from November 1989 to 1994. Ray left QPR in the summer of 1994 on a free transfer to join Crystal Palace as a player-coach under manager Alan Smith, but only made one appearance due to breaking his left foot on his debut.

He re-joined QPR as player-manager on 15 November 1994, following the exit of Gerry Francis. As player-manager, he appeared in a further 21 games for the club from 1994 to 1996. He left QPR by mutual agreement in September 1996 after the club was bought by media tycoon Chris Wright following their relegation from the FA Premier League.

Ray played for four clubs in the 1996–1997 season. He played one game at Wycombe Wanderers before moving to Hibernian for a 16-game stint. Toward the end of the season he played three times for Millwall in the Second Division and, finally, three Third Division games for Leyton Orient before retiring.

Wilkins scored three goals in 84 games for England, captained the team on ten occasions and played at the 1982 and 1986 World Cups. Ray was called up to play for England for the first time in 1976 by coach Don Revie, then made his debut on 28 May in a 3–2 win over Italy at the U.S.A. Bicentennial Cup Tournament in New York.
He made his 84th and final England appearance in November 1986, against Yugoslavia.

Ray was QPR manager from 1994 to 1996, and managed fellow West London club Fulham in 1997–1998. In March 1999, Ray was appointed Chelsea's first-team coach as interim manager after the sacking of Gianluca Vialli at the start of the 2000–01 season He was sacked from the club on the orders of new manager Claudio Ranieri in November 2000.

When Vialli was hired by First Division club Watford, Ray again assisted him until their dismissal in June 2002. From 2003 to 2005, he assisted former Chelsea player Dennis Wise in his managing of Millwall, but announced his exit when he took exception at Dave Bassett being hired in the coaching staff.

From 2004 Ray was assistant coach to Peter Taylor with the England under-21s until Taylor left in early 2007. Ray was not retained by incoming head coach Stuart Pearce.

In September 2008, he was appointed assistant first team coach to Luiz Felipe Scolari at Chelsea, following Steve Clarke's departure to West Ham United F.C. In February 2009, following Scolari's shock sacking, Ray was appointed as Chelsea's caretaker manager for the Fifth round FA Cup tie with Watford.

On 11 November 2010, it was announced that Ray's contract with Chelsea "would not be renewed" and that he was to leave the club "with immediate effect". On 1 December 2010, Ray reached what he described as a "harmonious conclusion" with Chelsea following his unexpected departure from Stamford Bridge.

Chelsea manager Carlo Ancelotti, who was himself sacked at the end of the 2010–2011 season, wrote about Wilkins, in his autobiographical book The Beautiful Games of an Ordinary Genius: "Ray is one of those select few, always present, noble in spirit, a real blue-blood, Chelsea flows in his veins ... without him we wouldn't have won a thing."

On 30 December 2013, Ray was appointed assistant head coach of Fulham. He and technical director Alan Curbishley were sacked on 17 February 2014 and the season ended with relegation.

On 3 September 2014, Ray was appointed as the new head coach of Jordan. He led Jordan at the 2015 AFC Asian Cup, where they were eliminated in the group-stages for the first time after two losses against Iraq and Japan and a win over Palestine.

On 25 June 2015, Aston Villa manager Tim Sherwood appointed Ray as his assistant manager. On 26 October 2015, he was sacked along with Tim Sherwood and the rest of the coaching team.

In the 1990s Ray was part of the team that contributed to the Football Italia show that aired on Channel 4. He later appeared as a commentator for Sky Sports, particularly on their Champions League coverage. He also worked for Talksport.

Ray was a patron for the charity Cardiac Risk in the Young. In 1993, he was made an MBE.

On 28 March 2018, Wilkins had a cardiac arrest resulting in a fall and was placed into an induced coma at St George's Hospital in Tooting.

Hours after his death, Milan played rivals Inter Milan in the Derby della Madonnina at the San Siro. His former captain Franco Baresi laid a bouquet of flowers next to Wilkins' shirt by the side of the pitch. A section of Milan fans held aloft a banner which read "Ciao Ray: Leggenda Rossonera" (English: "Goodbye Ray: Legend of the Red and Blacks"). During Chelsea's home game against West Ham United on 8 April, fans at Stamford Bridge gave a minute's applause in the eighth minute to pay tribute to Ray. They also held a banner which read "Ray was one those select few, he knew what it meant to be one of us a real blue blood. Chelsea flowed through his veins, may you rest in peace Ray."

A memorial service was held for Wilkins on 1 May at St Luke's Church, Chelsea, attended by many figures who knew him from the world of football.