Slough Town had their first ever league success in 1951, when they won the Corinthian League. For the rest of the fifties they were limited to cup success, winning the Berks & Bucks Senior Cup in 1955, and the Berks & Bucks Benevolent Cup four times.

In 1963, the Corinthian League became Division 1 of the Athenian League, and two years later Slough Town were promoted as champions. Three years after that they won the Premier Division.

The early seventies were Slough Town's most successful period so far, and they had eight amateur internationals on their books. In 1972 and 1973 they won the double of Athenian League and Athenian League Cup, and they also won the Berks & Bucks Senior Cup in 1971 and 1972. In 1973 they reached the final of the FA Amateur Cup, losing 1-0 to Walton & Hersham.

In 1973, Slough Town joined Division 1 of the Isthmian League, and in their first season were promoted to the Premier Division as runners-up.

For many years Slough Town had been tenants at the Slough Greyhound Stadium, but in 1974 they were required to leave, so they moved to Wexham Park. Their accumulation of trophies continued, as they won the Isthmian League Cup in 1976, and the Berks & Bucks Senior Cup in 1977. In 1981 they were Isthmian League champions for the first time, completing the double by winning the Isthmian League Cup for the second time. The Berks & Bucks Senior Cup was also won, making this the most successful year in their history.

The eighties did not see any more trophy success, but the club did reach the second round of the FA Cup in 1980, 1983, 1986 and 1987. Their finest moment was in 1983, when they beat 3rd Division Millwall in the first round. Their FA Cup success continued, with eight first round appearances in the nineties.

The trophy drought ended in 1990 with a second Isthmian League title, and this gained them promotion to the Conference, the top level of non-league football.