Inverness Thistle Football Club was founded in 1885 and was a member of the Inverness Combination Association. In 1888 they became one of the founding members of the North of Scotland F.A. and the following year the team was strengthened by the integration of Crown F.C. Inverness Thistle F.C. won their first trophy, the Inverness Charity Cup, in 1890-91. In 1893 the Highland Football League was formed and in the inaugural season Inverness Thistle F.C. won their first of eight championships. The club was strengthened further in 1895 by the simulation of Inverness Union F.C. and the move to a new ground, Kingsmills Park, followed shortly after.

Inverness Thistle competed in the Highland Football League for the next 80 years and in 1973 the club narrowly failed to claim a place in the Scottish League, losing out to Ferranti Thistle (now Livingston F.C.), by a single vote.After a long and illustrious history as member's of the Highland League Inverness Thistle F.C. won their last trophy, the Inverness Cup, in the club's final season (1993-94) .

Appropriately, the last game ever played by Inverness Thistle F.C. was a Highland League game at Kingsmills Park on the 14th May 1994. In the summer of 1994 the club merged with local rivals Inverness Caledonian F.C. to form the Scottish League side Caledonian Thistle F.C. (later Inverness Caledonian Thistle F.C.). Inverness Thistle was to be consigned to the history books and the memories of their fans.