In 1921–22, together with Shelbourne, Bohemians, Jacobs, Frankfort, Olympia, YMCA and Dublin United, Gate became founder members of the League of Ireland. Like Gate, the other seven founding members had spent the 1920–21 season playing in the Leinster Senior League. Gate initially emerged as one of the strongest teams in the league and in their debut season won a treble. In addition to winning the inaugural league title, they also won the 1921–22 FAI Cup and the 1921–22 Leinster Senior Cup. This season proved to be the highlight of Gate's time in the League of Ireland. In 1939–40 they won a second league title, however after finishing in last place in 1943–44 they failed to gain re-election. It had been suggested that the reason for this was the club announcing its intention to revert to amateur status. However, when the vote was being taken, the representative for Shamrock Rovers stated, "the St. James's Gate club has not full control over their own finances, as any profit made during the season goes to the Guinness Athletic Union and is therefore lost to football." The other clubs were also known to be unhappy that members of the Guinness Athletic Union did not have to pay into home matches, depriving those clubs of their share of gate receipts.
In 1990–91 Gate joined the League of Ireland First Division, replacing Newcastlewest. In 1995, the club was taken over by a consortium. Only one year later, however, just before the start of the 1996–97 they pulled out of the league, unable to meet their financial responsibilities. They were replaced by St. Francis.
110th Anniversary Tournament
To celebrate their 110th anniversary, in July 2012 the club hosted a tournament.
Semi-finals
Third place play-off
Final
Grounds
Gate originally played their home games at Bellevue Lodge by the Grand Canal near Inchicore. The same venue was also used by Olympia. Between 1921 and 1928 they played at St. James's Park in Dolphin's Barn on a pitch hired by the Guinness board. In 1928 they moved to their current home at the Iveagh Grounds.
Notable former players
;Republic of Ireland internationals On 28 May 1924 when Ireland made their international debut at the 1924 Olympics against Bulgaria, the Ireland team included three Gate players – Paddy Duncan, Michael Farrell and Ernie MacKay. A fourth member of the team, Paddy O'Reilly, would also later play for the club. Duncan also scored the Republic of Ireland's first international goal. Joe O'Reilly, with 20, was also the most capped player for Ireland in the pre–Second World War era. ;Republic of Ireland women's internationals
;Ireland internationals In addition to playing for Ireland teams selected by the FAI, at least five Gate players also played for Ireland teams selected by the Irish Football Association.
;Goalscorers On seven occasions St James's Gate players finished as the League of Ireland's top goalscorer. On 30 March 1930, Willie Byrne scored six goals in a 7–1 win against Sligo Rovers. Paddy Bradshaw, with 68, remains Gate's top goalscorer in the League of Ireland.
