Smith began his career with Scottish Premier League side Celtic. He made his début aged 17 and played 22 games, including two Old Firm matches, between 1991 and 1995.
Dundee
Smith never gained a regular place at Celtic Park and joined fellow Scottish side Dundee in August 1995. He quickly established himself in the team at right-back and was made club captain in 1997, the same year Dundee achieved promotion to the Premier Division. After playing with the Dens Park side for ten-and-a-half seasons, Smith reached his testimonial year. He also took on the role of joint caretaker manager for the final two games of the 2005–2006 season following the dismissal of Alan Kernaghan.
Valur
At the end of the 2005–2006 season, Smith transferred to Icelandic outfit Valur, helping them to third place and winning the Icelandic Premier Division, their first championship in 20 years.
Partick Thistle and Greenock Morton
During the Icelandic close season, Smith was loaned back to Scottish clubs. In January 2007, he joined Partick Thistle, making 18 appearances and scoring one goal, while in January 2008 he joined Greenock Morton, making 5 appearances until he underwent a cartilage operation which kept him out for the rest of the season.
Return to Dundee
On 4 November 2008, Smith returned to Dundee as U19 coach, with his registration as a player following in January, whereupon he was loaned out to neighbours Brechin City, with the ability to be recalled at any time. Brechin City's status as a part-time team enabled Smith to continue in his role as U19 Coach at Dens Park.
Coaching career
Dundee
On 15 October 2010, Smith was appointed manager of Dundee. He succeeded Gordon Chisholm, who had been made redundant after the club entered administration. Smith led the team to a club record unbeaten league streak of 23 games, guiding Dundee to safety despite the team receiving a 25-point deduction for entering administration for the second time in seven years. This was rewarded, on 10 May 2011, when Smith signed a new three-year deal at Dundee, contracting him as manager until the end of the 2013–14 season. Despite finishing second in the 2011–12 Scottish First Division, Dundee were admitted to the Scottish Premier League due to the liquidation of Rangers. Dundee struggled in the early part of the 2012–13 Scottish Premier League, winning three out of 22 matches. Despite this, the Dundee board restated their backing for Smith, citing the difficulty in adjusting to the SPL in unusual circumstances. However, just 47 days later, Smith and Dundee parted company. His sacking was criticised by St Johnstone manager Steve Lomas, believing Smith deserved another chance.
Alloa
On 1 July 2013, Smith joined Ross County as the club's Under-20s coach. In January 2014, Smith was appointed manager of Scottish Championship club Alloa Athletic. He guided Alloa to the final of the 2014–15 Scottish Challenge Cup. Alloa defeated Rangers in the semi-final, with Smith noting the fact he had become the first Alloa manager to win a match against Rangers. Smith said in December 2014 that he hoped to return to a full-time management job. After a run of one win in 13 matches, he resigned as Alloa manager in March 2015.
Aldershot
On 27 April 2015, Aldershot Town appointed Barry Smith as their manager. He resigned a year later due to family issues.
East Fife
Smith was appointed manager of Scottish League One club East Fife in December 2016. He left the club on 30 May 2017.
Raith Rovers
After leaving East Fife, Smith took over as manager of recently relegated Scottish League One side Raith Rovers on 30 May 2017. Rovers finished second in 2017–18 Scottish League One, narrowly missing out on automatic promotion and then losing in the playoffs to Alloa. Smith resigned from his position on 4 September 2018, with the team sitting in second place.
Brechin City
Smith was appointed Brechin City manager in November 2018. On 13 July 2019, Smith was forced to play himself in a League Cup game against Forfar Athletic due to a shortage of players, nine years after retiring from playing. Smith left Brechin on 19 August 2019, after they had lost their first three matches of the 2019-20 Scottish League Two season.
Forfar and Dundee return
Smith was made assistant manager for Forfar Athletic underneath manager Jim Weir in October 2019. During Smith's short tenure with the Loons, Weir was recovering from a car crash, and eventually had to resign due to complications caused by the crash. As part of a new change in management, Smith left Forfar shortly after. Smith made his return to Dundee a couple of weeks later, taking up a role in the club's academy headed by Gordon Strachan and Stephen Wright.