In my opinion, Norwich's defence has never been as solid since the departure of Ian Culverhouse. The right back position was not adequately replaced and this problem need not have occurred if Robert Chase's Norwich regime had been willing to discuss contracts in a sensible manner. From being an integral part of the City team that finished third in the Premiership and enjoyed UEFA Cup success, Ian Culverhouse found himself at the start of the 1994-95 season, out of contract and out of favour with Robert Chase and manager John Deehan. Similar problems had occurred the previous season with Dave Phillips. Ian's outburst at being dropped from the first team squad offended the powers-that-be at Carrow Road and destroyed what chance he had of regaining a first team position. Mark Robins and Mark Bowen would suffer similar fates. Despite injuries in October 1994 to his replacement Carl Bradshaw and youngster Johnny Wright, Ian was still not recalled to the first team and eventually was transferred to Swindon for the bargain sum of £150,000 in December 1994, the fee being fixed by a tribunal. Ian's career was rejuvenated in Wiltshire and he had made 97 league appearances for Swindon by the end of the 1997/98 season.

Ian Culverhouse began his career with Tottenham Hotspur and made just 2 league appearances for the Spurs before joining Norwich in October 1985 for £50,000. His career improved as he became a first team regular and had made 369 appearances for the Canaries before he fell from grace and out of the first team. He won the Division Two championship in his first season, reached two FA Cup semi finals, finished in the top five of the old First Division, finished third in the Premiership's inaugural season, played in Europe and won the Club's Player-of the-Year award in 1990/91.

The Swindon Town Official website revealed that Ian was given a free transfer by The Robins on transfer deadline day 1998. No league club showed any interest then in his services and he only signed up with a team in July 1998. After a two week trial with Stevenage, he joined Kingstonian and played in a pre-season victory over Nottingham Forest on 30th July. He played for Kingstonian on the opening day of the Vauxhall Conference season but joined Brighton on a short term contract shortly afterwards. He made his debut on 19th August against Northampton in the Worthingtons Cup. He was playing alongside former teammate Mark Walton. Ian then took over the responsibility of managing the Brighton reserve team thus making fewer appearances for the first team.

Ian joined Barnet as Youth Team manager in the summer of 2000 but was not been registered as a player. Unfortunately for Ian, Barnet were relegated into the Conference on 5th May 2001. In January 2002, Ian moved across London to join Leyton Orient as their youth coach. He was later promoted to Assistant Manager. Orient manager Martin Ling instigated a shake-up at the end of the 2004/5 season which saw Culverhouse leave the club and replaced by youth team coach Dean Smith. Ian wasn't out of the game for long, joining Wycombe Wanderers as their youth team coach at the end of July 2005. He was promoted to first team coach in June 2007

On 10th October 2008, it was announced that Culverhouse had been appointed as Assistant Manager to new Colchester boss Paul Lambert who Culverhouse knows from their time together at Wycombe.

When Lambert was appointed Norwich manager on 18th August 2009, Culverhouse resigned from his position at Colchester to take up a similar role at Carrow Road.

At the end of their first season, Lambert and Culverhouse enabled Norwich to win the League One title. The following season, they won promotion to the Premier League. Norwich finished 12th in their inaugural season back in the Premiership. When Paul Lambert quit Norwich to take charge at Aston Villa, Culverhouse and Gary Karsa followed him, departing the club on 5th July 2012.

In ”It’s great for them to be here at the club and I’m delighted they have joined me” said Lambert. ”They have been with me for the past six years which is a long time and we’ve built up an understanding and a trust. I trust them and they have been great for me. We have always bounced well off each other and we’re all looking forward to the job at hand here at Villa.”

In April 2014, Karsa and Culverhouse were suspended by Villa after being accused of bullying and aggressiveness by players and other staff members. They were sacked in May 2014.

In September 2015, he was linked with the managerial vacancy at Peterborough along with former Liverpool forward Robbie Fowler.

Culverhouse joined Dagenham & Redbridge in January 2016 as John Still's assistant but they could not avoid the Daggers being relegated to the Conference in April 2016.

On 22nd February 2017, Culverhouse left Dagenham to become the new manager of Kings Lynn Town after the Linnets had sacked Gary Setchell. The Daggers were sitting second in the Conference when Culverhouse left.

Culverhouse announced in April 2017 that he would leave Lynn at the end of the season. He held to this even though he led Lynn to the Southern League play-off final which was lost 2-1 to Slough on 7th May 2018. He had been linked with the Cambridge vacancy. Instead he was announced as the new manager of Grantham Town on 30th May 2018; a surprising move considering that Lynn and the Gingerbreads play in the same division. Grnatham chairman Roger Booth said “I’m delighted Ian has agreed to become our manager We hope he can build on the momentum the club has, things are happening in all areas of the club and everyone associated with it has every right to be positive about the clubs future."

Culverhouse quit Grantham on 17th October 2018 after they slipped to their fifth consecutive league defeat. Culverhouse surprisingly returned to Kings Lynn as Manager on 1st November 2018. He will be assisted at The Walks by former Boston United goalkeeper and UK appearance record holder Paul Bastock. They replace the joint management team of Neil Fryatt and Robbie Back who have taken up new positions within the club. At the end of the 2018/19 season, Culverhouse led Kings Lynn to promotion. Finishing second in the Southern League, they got through the play-offs to face the winner of the Northern Premier League play-offs. This was Warrington whom the Linnets defeated 3-2 in extra time on 11th May 2019, securing a place in the National League (North) for 2019/20.

On 17th June 2020 it was confirmed that Kings Lynn were the winners of the National League North, The Linnets finished the curtailed campaign second in the table, two points behind York City but crucially, with two games in hand. Lynn last played a game back in March, when football was brought to a halt by the coronavirus pandemic. Since then there had been numerous delays as the National League Board awaited the outcomes of voting in Leagues One and Two and the subsequent consultation with their own clubs. Following a vote by all member clubs, and subject to FA Council approval, it was decided that the Vanarama National League, Vanarama National League North and Vanarama National League South seasons 2019/20 will be concluded with final league tables compiled on an “Unweighted Points Per Game” basis. This put Lynn ahead of York City to win the title and promotion into the National League.

On 29th November 2021 he was sacked by Lynn on the back of a run of eight league defeats in a row which has left the Linnets second from bottom of the National League and struggling for survival. The club said: "King’s Lynn Town FC can confirm that following a number of meetings and discussions over the past few days between club chairman Stephen Cleeve and the manager Ian Culverhouse, that a mutual agreement has been reached for Ian Culverhouse to leave his role as manager of the club. Club chairman Stephen Cleeve and Ian Culverhouse both agreed this action is in the best interest of the club going forward."

On 23rd January 2022 Culverhouse returned to management taking charge of Kettering Town with Paul Bastock again supporting him. He left the club in May 2022.

On 6th September 2022 he was appointed manager of National League North side Boston Town.