In the mid to late 1960s, Town built up a rivalry with fellow Bridlington side Bridlington Trinity. During the 1966-67 season in the Yorkshire League, Town won the championship while Trinity finished second. The following year it would be Trinity who took the title and Town finished in third. This rivalry continued until the early 1970s when Trinity became part of the Midland League.
By 1986-87, they were promoted to the Northern Counties East League Premier Division, even though they only finished sixth. This was because several teams in the Premier Division had resigned in the close season. This gave Town the opportunity to ignite their old rivalry with Bridlington Trinity, for the first time since the early 1970s.
During the first three seasons in the Premier Division, Town finished higher. With a third and a fourth place, while Trinity were in the bottom half. The 1989-90 season was the concluding showdown for the two clubs. Town were crowned champions, while Trinity ended the season a respectable fourth. This would prove to be the end of the rivalry as Trinity folded due to the termination of their groundshare with Bridlington Town. Unfortunately for Bridlington, they were unable to put the icing on the cake in their FA Vase final clash at Wembley with Yeading F.C., they drew the game, but lost in the replay 1-0 at Elland Road.
Town marched on to the Northern Premier League Division One. The 1992-93 season was the most successful in the clubs history, they finished as champions of the NPL Division One, and they finally took the FA Vase at Wembley, beating Tiverton Town 1-0. Alan Radford scored the only goal of the game.
The sunny spell would not last, due to legalities, the team were forced to play their home games at Doncaster Rovers' ground; Belle Vue. The club went into turmoil. They finished 21st in the Northern Premier League Premier Division and were deducted three points. Instead of going into Northern Premier League Division One, they folded.
The Greyhound club agreed and a new club crest was designed and a new motto "Pergere et Eniti", which means "Onwards and Upwards". The club returned on 10 September 1994, and were put into the league where they had originally played during their formative years; the Driffield and District League, it was literally back to square one.
Bridlington progressed steadily, gaining entry to the East Riding County League Division One, they won the league and cup double. After three seasons in the East Riding County League Premier Division, Town finished runners-up and applied for promotion back into the Northern Counties East League Division One. They were accepted and spent three seasons at this level; finishing fifth, and then fourth, before achieving promotion with a runners-up spot in 2001-02.
Town made their mark in 2002-03, reaching the quarter-final of the FA Vase before going out to Brigg Town. And they also reached the Fourth Qualifying Round of the FA Cup, eventually losing to Conference National side Southport. Bridlington Town won the league that year, they were crowned champions with 20 points ahead of the runners-up.
In 2007, it was announced that Bridlington Town would play in the inaugural season of the Northern Premier League Division One North. However a disastrous campaign followed, and they finished bottom of the division, and were relegated to the Northern Counties East League Premier Division.