He found first team opportunities limited there and made just two league appearances for the club, though he did get a winner's medal in the UEFA Cup as he was an unused substitute for Spurs in the 1984 final against Anderlecht.
After injury during end of the 1986–87 season, Culverhouse found himself contesting a first team spot with the manager's son Kenny Brown at the start of the 1987–88 campaign.
[3] After Brown was replaced by Dave Stringer Culverhouse regained his first team place and attained a level of performance and consistency that made him a fixture in the starting eleven for the best part of a decade.
Culverhouse acquitted himself well on the European stage, playing as a sweeper in a system introduced by manager Mike Walker for the European campaign,[4][5] although he missed the away leg at Inter Milan's Giuseppe Miazza stadium – the match that saw City eliminated from the UEFA Cup – due to suspension, having picked up two yellow cards in the competition.
He was sold to Swindon Town for £150,000 in December 1994, having lost his regular place in the Carrow Road first team to new signing Carl Bradshaw at the start of the season.
[9] Having worked with Paul Lambert at Norwich City, Wycombe Wanderers, Colchester United and then Aston Villa, the duo were now separated.
Despite being relegation favourites and suffering a 3–0 defeat to Guiseley on the opening day of the season; Culverhouse and his team defied the odds and found themselves embroiled in a promotion battle with York City.
When the season was suspended in March 2020 due to the COVID-19 outbreak; King's Lynn were in 2nd position, two points behind York but crucially had two games in hand.