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After winning back-to-back League of Ireland Premier Division titles with Dundalk, McGrath signed a ​2  ⁄2 -year deal with Scottish Premiership side St Mirren on 7 January 2020.

Professional appearances – correct as of 11 March 2020

McGrath moved from St Patrick's Athletic to Dundalk for a transfer fee on 15 January 2017.

Although he struggled with shin splints that kept him out of games at the beginning of the 2016 season, his importance to the team increased in a season where the team struggled to deal with the midfield losses of Chris Forrester, Greg Bolger, Killian Brennan and James Chambers. Those losses however, created an opportunity for McGrath to play a lot of games in the role of attacking midfielder throughout the season. His first goal of the season was an 89th-minute strike to rescue a point at home to relegation fighting Longford Town live on Eir Sport. His only appearance in Europe for the season came against Dinamo Minsk of Belarus as Pats lost 1–0 at home and were knocked out of the Europa League in the second qualifying round. McGrath played a huge part in the Saints retaining their League Cup trophy as he played in every game, scoring away from home against Bray Wanderers in the quarter finals, Shamrock Rovers in the semi's and Limerick in the Final. Following a good season for McGrath, he was voted St Patrick's Athletic Young Player of the Season by the club's supporters.

McGrath's first taste of under-19's international football came when he was called up to the Republic of Ireland under-19s by Paul Doolin for their November 2014 games against Malta and Gibraltar. His first appearance came against Malta in a 1–0 win in Waterford. He went on to make a total of 6 appearances for the 19's, scoring twice vs Azerbaijan at Tallaght Stadium. McGrath was called up to the Republic of Ireland under-21 squad for the first time by manager Noel King on 8 November 2016, for their games against Czech Republic and Slovakia in La Manga Club, Spain.

He was named as a first team player ahead of the 2015 season, with number 19 being assigned to McGrath as his squad number. Mid season when first choice striker Christy Fagan picked up a knee injury, McGrath had an extended run in the starting 11 as a striker and scored his first goals away to Drogheda United and Sligo Rovers in consecutive away games to secure 2–0 and 3–0 wins respectively. McGrath made his first appearances in UEFA competition when he came on from the bench both away and at home against Latvian side Skonto Riga in the Europa League. McGrath came on at the start of extra time in the 2015 League of Ireland Cup Final as Pats drew 0–0 with Galway United before winning 4–3 on penalties to win the League Cup at Eamonn Deacy Park. McGrath received rave reviews from fans, pundits and the media alike for his breakthrough season, coming in a second behind Lee Desmond in the club's Young Player of the Year awards and also being voted into pundit Dermot Keely's team of the season in his article in The Irish Sun.

A native of Athboy, County Meath, McGrath played youth football for his local club Athboy Celtic before joining top Dublin youth side Cherry Orchard. He played for UCD under 19's before joining St Patrick's Athletic under 19 side on their scholarship scheme with NUI Maynooth. He played for Pats under 19's for two seasons, including a league winning campaign in which McGrath scored two goals against Derry City under 19's in the final. He progressed into the first team in 2014 whilst still playing for the club's under 19 side.

McGrath made his senior debut with the first team on 9 September 2014 as he played the full 90 minutes in a 2–1 win over Longford Town in the 2014 Leinster Senior Cup Final at City Calling Stadium. McGrath impressed Saint's fans with his display, including an excellent through ball to set up Jack Bayly's winning goal in the 64th minute. His League of Ireland debut came on 17 October 2014 when he started against Athlone Town in a 2–0 loss at Richmond Park.

Jamie McGrath (born 30 September 1996) is an Irish professional footballer playing for Scottish Premiership club St Mirren, having previously played for Dundalk and St Patrick's Athletic.