Aldershot F.C. were among the founder members of the Fourth Division in the 1958–59 season. The club twice reached the fifth round of the FA Cup, once in its inaugural Football League season and once in 1978–79. An FA Cup match against Carlisle United on 28 January 1970 saw Aldershot's record attendance of 19,138. Teddy Sheringham played for Aldershot six times while on loan to the team from Millwall in 1985. Their most recent success was in the 1986–87 season, when they became the first winners of a play-off final, beating Wolverhampton Wanderers over two legs to gain promotion to the Third Division, but they were relegated back to the Fourth Division two years later. In August 1990 they were wound up in the High Court, 'hopelessly insolvent' with debts of £490,000. They were then saved from closure by 19-year-old self-styled property developer Spencer Trethewy.
Their manager at this time was Len Walker, who took over in June 1985, achieved promotion in 1987 and was retained after relegation in 1989. He became general manager in March 1991 on the appointment of Brian Talbot as player-manager. Talbot remained in charge of the Shots for just eight months before being replaced by Ian McDonald, who was at the helm for four months leading up to Aldershot's bankruptcy.
On 25 March 1992 Aldershot F.C. finally went out of business and were obliged to resign from the Football League. The final game played was against Cardiff City at Ninian Park, five days before the club went out of business. Aldershot's league record for the 1991–92 season was expunged; they were bottom of the league at the time of their resignation.
In response to the bankruptcy a group of supporters set up a new club, Aldershot Town F.C., which started in the Isthmian League Division Three, five levels below the division in which Aldershot F.C. had been playing. Aldershot Town won promotion to the Football League on 15 April 2008 by winning the Conference National.