McGinlay is perhaps best known for his five-year spell with Bolton Wanderers between 1992 and 1997, where his scoring exploits led to him being nicknamed 'Super John'. After his goals eliminated FA Cup holders Liverpool from the competition, he successfully partnered fellow Scot Andy Walker as the Trotters gained promotion from the third tier in 1993, with McGinlay scoring the match winning penalty in the last fixture against local rivals Preston North End. Further cup 'giant killings' over teams such as Everton and Arsenal followed the next year, with McGinlay featuring prominently – he scored 33 goals across all competitions during the campaign, and the team became known in local media as 'white hot' due to the performances. In the 1995 he was in the side which gained promotion to the Premier League via the play-offs, playing all 120 minutes of the dramatic 4–3 victory over Reading, and also started in the League Cup Final in the same season. In April 1997, he scored the last goals at Burnden Park, finishing as the club and the division's top scorer with 24 goals from 43 games as Bolton returned to the top level, this time as champions. He scored a hat-trick in a 6–1 cup win over Tottenham Hotspur. He made seven further league appearances for the club at the outset of the next season before joining second-tier Bradford City in November 1997 for £625,000 in what would be an injury-hit move. He later had the Bolton club crest tattooed on his arm.
Later years
McGinlay had short spells with Oldham Athletic and American team Cincinnati Riverhawks before moving into management with non-league sides Ilkeston Town and Gresley Rovers. In 2013, he was also employed as a chief scout by Wigan Athletic, appointed by former Bolton teammate Owen Coyle during his spell as manager, after spending time working in similar roles in the US with Cincinnati Kings, and with the Scottish Football Association. In 2014, McGinlay took over the 240-year old Horwich pub the Original Bay Horse. He rejoined Bolton Wanderers in an official ambassadorial role in 2020, in an attempt by the club to strengthen their ties with the sports courses held at the University of Bolton, and to bring former players back into contact with the club.
International
During his time with Bolton, McGinlay earned 13 international caps for Scotland, scoring four goals; his last and most important strike was the only goal of a 1–0 victory over Sweden and helped the national side qualify for World Cup 98, although he did not make the squad for that tournament, nor for the Euro 96 competition. McGinlay lined up for Scotland alongside his childhood friend from Fort William, Duncan Shearer, who also spent much of his career in England – the two never played in the same team at club level. He also featured in the infamous '3-second match' in Estonia and its replay in Monaco, and missed the birth of his daughter in order to travel to Belarus for another qualification game the following year.