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Leighton became Aberdeen's goalkeeping coach after retiring as a player. He parted company with the club in August 2009 when manager Mark McGhee (his former teammate, who had also brought him to Reading years earlier) chose to replace him with Colin Meldrum. In February 2010 he was appointed as goalkeeping coach for Huntly in the Highland League. Leighton was reappointed as the goalkeeping coach at Aberdeen on 13 December 2010, the first act of the new management team of Craig Brown and Archie Knox; he left the club again at the request of manager Derek McInnes, at the end of the 2014–15 season. He commented soon afterwards that he would look for work outside football, as he was unwilling to relocate from Aberdeen due to other work and family commitments, and subsequently became a sales manager for companies providing services to the city's offshore industry.

He retired from playing after the 2000 Scottish Cup Final defeat by Rangers. In that game he was substituted after three minutes, suffering a broken jaw in a challenge from Rod Wallace (requiring the insertion of metal plates into his face). With no substitute goalkeeper available, forward Robbie Winters took over in goal and Aberdeen lost 4–0. Leighton's final league appearance that season meant that he set the record for the oldest player in the Scottish Premier League at 41 years and 302 days (since broken by Andy Millen in 2007).

In July 2000 he was given a testimonial against Middlesbrough, the same opponent as in his first appearance for Aberdeen in a 1978 friendly; however he could not actually play in the match due to recovering from his cup final injury. He released his autobiography the same year. In 2004 he was inducted into the club's Hall of Fame.

He retired from international football on 10 October 1998. His last match was a European Championship qualifier against Estonia when aged 40 years and 78 days. This set a new record as the oldest player to play for Scotland, since broken by David Weir in September 2010. Leighton is a member of the Scotland Football Hall of Fame, having won his 50th caps in 1989. Leighton played 91 times for Scotland, second only to Kenny Dalglish's 102 appearances.

In 1997 Leighton returned to Aberdeen, where he featured regularly for another three seasons and reached 500 appearances for the club in 1998. He was captain in the 2000 Scottish League Cup Final defeat to Celtic.

After Leighton fell out of favour at club level, Andy Goram became Scotland first choice goalkeeper and played at Euro 92 and Euro 96. Leighton regained the position after a man of the match performance in a 1-0 home win versus Sweden in November 1996 during qualification for the 1998 World Cup. Leighton played all three Scotland matches at the tournament finals.

His career was revitalised after Alex Miller signed him for Hibernian in summer 1993, Leighton playing over 150 games and missing only one league match in four seasons. He played in the 1993 Scottish League Cup Final) defeat to Rangers. He was recalled to the Scottish national team, collecting 23 of his 91 Scotland caps at Hibs. He later said he played the best football of his career in his spell at Easter Road and rated Miller the second-best manager he played under.

In March 1992 Iain Munro signed him for Dundee for a £200,000 fee. He played in the last dozen league games of the season winning the title in the Scottish second tier and promotion to the top flight. He was out of favour at Dens Park after Simon Stainrod replaced Munro as manager. Leighton had another non-playing loan spell at Sheffield United.

Leighton remained fourth choice United keeper in season 1991–92 behind Peter Schmeichel, Walsh and youngster Ian Wilkinson. He spent a portion of that season on loan with third-tier Reading.

Sealey retained the position of first-choice goalkeeper for the 1990–91 season after signing a permanent contract. Although Leighton remained contracted to United for nearly two more years, he played only one more game for the club (against Halifax Town in the Football League Cup on 26 September 1990). He was fourth choice keeper in 1990–91 behind Sealey, Gary Walsh and youngster Mark Bosnich, and was loaned to Arsenal between March and May 1991, a period in which they won the league title, although he did not play.

In 1989–90 United finished two places lower in the league in 13th. Leighton played when United were defeated 5–1 in the league by newly promoted neighbours Manchester City,and conceded three goals in 1990 FA Cup Final, a 3–3 draw with Crystal Palace. He was then dropped from the United starting lineup for the replay, in which Les Sealey made a number of saves as United won the match 1–0. Leighton's disappointment was such that when handed the winner's medal by Sealey, he later returned it to his replacement's pocket, and when a medal specifically for Leighton was received by the club due to his appearance in the first match, he declined that too. The two players remained close friends, although Leighton's relationship with Ferguson deteriorated to the point where the two were no longer on speaking terms.

Ferguson, who had left Aberdeen to manage Manchester United in 1986, signed Leighton for £500,000 in 1988. In his first season with United, the club finished 11th. Leighton conceded 35 league goals and kept 14 clean sheets, while he conceded more than two goals only once in all competitions.

Leighton played in 91 international matches for Scotland. He was chosen for FIFA World Cup squads in 1982, 1986, 1990 and 1998, playing in the latter three of those tournaments.

Leighton's international career lasted for 16 years, from 1982 to 1998. He was an uncapped squad member for the 1982 World Cup, before making his debut against East Germany on 13 October 1982. Within two years he was his country's No. 1, and he played in all of his country's matches at the 1986 and 1990 World Cups.

Leighton joined Aberdeen from Scottish Junior club Dalry Thistle in 1977, after working in the civil service on leaving school. Before breaking into the Aberdeen first team he was loaned out for one season to Highland League club Deveronvale, where he is now an inductee of the club’s Hall of Fame. Leighton achieved his greatest success under the management of Alex Ferguson in the early to mid-1980s. With Leighton in goal, Ferguson's Aberdeen won Premier Division titles in 1984 and 1985, the Scottish Cup four times, the Scottish League Cup once, and the European Cup Winners' Cup and Super Cup in 1983.

Brian Clough, a notorious critic of others who backstopped for the national team during the 1970s and 1980s, has been reported as saying "Jim Leighton is a rare bird – a Scottish goalkeeper that can be relied on."

James Leighton MBE (born 24 July 1958) is a Scottish former footballer, who played as a goalkeeper. Leighton started his career with Aberdeen, where he won seven domestic trophies and the 1982-83 European Cup Winners' Cup under the management of Alex Ferguson. Ferguson then signed Leighton for Manchester United in 1988, but dropped him after he conceded three goals in the 1990 FA Cup Final. Leighton then had spells with Arsenal, Reading, Dundee and Sheffield United, and rebuilt his career after joining Hibernian in 1993. He returned to Aberdeen in 1997, leading to a career total of over 600 appearances in the league alone.