Goalkeeper John Ruddy signed for Norwich on 5th July 2010.

Ruddy began his professional career at Cambridge United and made his professional debut in the final game of the season at Leyton Orient's Brisbane Road stadium on 8th May 2004, noticeable for a clean sheet and penalty save. he made 39 league appearances for Cambridge, and had a trial at Manchester United before joining Everton in the summer of 2005 for a fee of around £250,000.

Whilst at Everton, he was called into the England Under-19 squad.

In September 2005, Ruddy signed for Walsall on loan, making four appearances in League One before being allowed to return to Everton. Loan spells with Rushden & Diamonds and Chester City soon followed.

Ruddy made his first team debut for Everton in February 2006, but in a rather bizarre way. Nine minutes into the match against Blackburn Rovers, Iain Turner was sent off for handling outside the area. Since Turner was substituting for injured first-choice and second-choice keepers Nigel Martyn and Richard Wright, it meant that Ruddy was the only keeper left who could play. Ruddy went on to keep a clean sheet in a 1–0 victory.

In September 2006, Ruddy was given another chance on loan. A one-month deal was agreed with Stockport County, which was extended to three months after an impressive performance. Since then he agreed another one month loan with Wrexham in February 2007 but failed to establish a place in the team during his time at the Racecourse Ground and the Red Dragons decided against extending the loan beyond the initial month. On 21st April, Ruddy completed an emergency one-week loan to League One side Bristol City and helped them move closer to promotion. In January 2009, he went out on loan till the end of the 2008–09 season at Crewe Alexandra.

On 24th July 2009, Ruddy joined Scottish Premier League side Motherwell on a six-month loan deal, to vie with Michael Fraser and Sebastian Kosiorowski for the number one jersey.. But when the original loan deal expired in January 2010, the Fir Park outfit decided that they wanted to keep Ruddy further and a month extension was agreed with Everton, whilst their futures were sorted out. On 27th January 2010, it was announced that both Ruddy and Everton teammate Lukas Jutkiewicz were to extend their stay at the Scottish Premier League side until May 2010

Ruddy made his Norwich debut in the 3-2 home defeat to Watford on the opening day of the 2010/11 season. His season improved and Norwich won promotion to the Premiership on 2nd May 2011 with a 1-0 win at Portsmouth. He finished the season with 46 appearances to his name.

Ruddy made 37 appearances in the Premier League during 2011/12 as Norwich finished 12th. His form saw him named as runner up in the Norwich City Player of the Year award. He was also linked with an England call-up which became reality when he was named in England's Euro2012 squad on 16th May 2012. However he had to drop out due to a broken finger sustained on the first day of international training.

Speculation linking Ruddy with a switch to Aston Villa was put to bed when he signed a four year contract with Norwich on 25th June 2012. Ruddy told the club’s official website: “I’m delighted. I have never wanted to leave Norwich since I’ve been here. I’ve had a great two years so far, and I can’t wait to be a part of it for the next four years. I love the atmosphere around the place and it’s a fantastic club to play for. We’ve a new manager coming in too, who I’m looking forward to working with. The main thing for me is that my family are really settled here as well. My lad starts school in September, so it’s nice to get a bit of security for them too. It’s been a non-stop rollercoaster since I joined, with a lot more highs than lows, thankfully, and hopefully that will continue over the course of the next four years.”

Norwich City boss Chris Hughton added: “I am delighted to have secured John’s future at the club for a further four years. He has been a key part of the club since he has arrived.He has made some fantastic progress over the past couple of years here and is an integral part of the club’s future.

John was selected for the England squad for the friendly game against Italy in Bern on 15th August 2012. He made his international debut coming on as a half-time substitute for fellow debutant Jack Butland. Ruddy kept a clean sheet, pulling off some good saves, as England won 2-1

On 28th November 2012, Norwich announced that Ruddy would be out of action for approximately three months due to a thigh injury sustained in the 1-0 win over manchester United but that had been worsened in the 1-1 draw at Everton. He returned to the first team for the clashes against West Brom (12th May) and Man City (19th May) which City won 4-0 and 3-2 to secure 11th place in the Premier League.

In mid-June 2013 he was linked with a move to Aston Villa and a reunion with Paul Lambert. On 28th June 2013, The Sun reported that Norwich had rebuffed a £5million bid for Ruddy from Chelsea.

He was ever present in Norwich's 2013-14 Premier League season, making 38 appearances. Despite Norwich's relegation at the end of the season, he was linked with moves to Crystal Palace and Arsenal, the latter reported to be preparing a £6m bid.

In December 2014, he was again linked with Crystal Palace but also with Everton who were considering him supposedly as a replacement for Tim Howard. He was also linked with Liverpool as a replacement for Simon Mignolet.

He made 50 appearances in the 2014/15 season as Norwich won promotion back to the Premier League with a 2-0 Championship Play-off final victory over Middlesbrough on 25th May 2015. After promotion, he was linked again with a move to Chelsea.

On 2nd May 2017, Norwich City announced that they would not be renewing the contracts of seven senior players in the summer including Ruddy. This was not due to ability but rather due to his wages. He was quickly linked with Championship rivals Aston Villa. He had played 29 games in 2016/17 taking his total to 243. He captained the Canaries in his final game, at home to QPR.

Ruddy was linked with a move to MLS side Vancouver Whitecaps, West Ham and on 30th June 2017 Aston Villa. Ruddy told the Daily Mirror that Steve Bruce’s Villa are an option. “Well, it’s a massive club with a superb infrastructure. Everyone knows Villa should be in the Premier League and I would love to be a part of making that happen.” He was then tipped for a move to Sunderland as the Black Cats are in the market for a new goalkeeper following the sale of Jordan Pickford to Everton and with just Mika and Vito Mannone as experienced keepers. On 7th July 2017, Ruddy was linked with Wolves following the diagnosis of leukaemia for keeper Carl Ikeme. This was finalised on 10th July with Ruddy signing a two year contract.

Ruddy was first choice keeper as Wolves secured promotion to the Premier League in 2017/18 in mid-April 2018. This was followed by the Championship title.

On 27th April 2020 it was reported in the Yorkshire Post that Ruddy would be joining Leeds when his contact with Wolves ends on June 30th 2020. His contract was extended until the summer of 2022 but on 24th May 2022 Ruddy confirmed he would be leaving Wolves. He had played 72 games for Wolves but 46 of them were in the Championship winning season of 2017/18.

On 14th July 2022 Ruddy signed a one year deal with Birmingham City.

Ruddy was in goal when Birmingham were relegated to League One on 4th May 2024 despite beating Norwich 1-0. Despite being offered a new contract, he announced on 27th June 2024 that he would be leaving Birmingham at the end of his contract. There were reports that he had spoken to Ben Knapper about a return to Carrow Road whilst other reports linked him with a reunion with former boss John Eustace at Blackburn Rovers as well as Charlton. On 1st July 2024 he signed a one year deal with Premier League side Newcastle United to act as cover even though the club had signed  goalkeeper Odysseas Vlachodimos from Nottingham Forest.

His son Jack signed a two year scholarship with Norwich in June 2024.