Seaford Town FC joined Sussex County League Division Two in 1952, and won promotion in 1963/64 after finishing as runners-up to Selsey. The next seven seasons were spent in the top division (finishing 4th in 1965/66) before being relegated back to Division Two in 1971.

In 1978 the club dropped out of the County League, but returned as founder members of the new Third Division five years later. In 1985/86 they returned to senior football as champions, and in 1988/89 took the Division Two title. However, their return to Division One was to last just two seasons before they were relegated once more in 1990/91. Worse was to follow, and in 1992/93 Seaford found themselves back in intermediate football again.

Things didn’t get any better, and Seaford dropped out of the County League altogether after being relegated in 1997. They spent two seasons in the East Sussex League before regaining their place in Division Three, having dropped the “Town” suffix in 1999 following a merger with Seaford Seagulls Youth FC.

Promotion back to Division Two was achieved in 2000/01, as runners-up to Rye & Iden United, with 6th place in 2004/05 their best finish since then. Prior to the 2005/ 06 season the name reverted back to Seaford Town, as did the colours from red and blue, to all red. The club finished in the top eight for the next three seasons, and their 6th place finish in 2006/07 bettered a similar finish in 2004/05 by one point.

With floodlights in place for the start of the 2008/09 season, Seaford were once again in a position to bid for a return to the top flight. That season Town were runners-up in the Division Two Cup, narrowly losing out to neighbours Peacehaven 1-0 in a keenly contested final at Shoreham Football Club.

Season 2009/10 proved to be disappointing in the league, with a heavy programme in the final month which saw them play no less than 11 games, was to be too much and they finished a disappointing 10th. But they once again proved to be an excellent Cup team, beating 4 Division One teams en route to the semi-final of the John O’Hara League Challenge Cup before losing a close faught game 2-1 to yet another top flight side in Crawley Down.