Republic of Ireland international winger Wes Hoolahan became Glenn Roeder's second signing of the 2008 pre-season when he transferred from Blackpool to Norwich on 26th June 2008, on a three year deal. Norwich had activated a get--out clause in Hoolahan's contract to sign him for £250,000. Norwich reserve team keeper, Matthew Gilks, moved in the opposite direction along with an undisclosed amount of money.

Hoolahan started his career at Shelbourne where he won three League of Ireland championships and excelled during their run in the Champions League qualifiers in the 2004-05 season. He was the PFAI Young Player of the Year in the 2002-03 season. He joined Scottish side Livingston but in July 2006, Hoolahan joined Blackpool on a season-long loan. This became a permanent transfer the following summer although Livingston denied agreeing to the deal and the transfer had to be approved by FIFA

Many Championship clubs invluding QPR and Charlton were linked with Hoolahan during the 2007/8 season but Norwich secured the deal seeking a replacement for Darren Huckerby.

Hoolahan, who had been capped at Under-21 level for Ireland, made his full international debut as a second half substitute in the 1–0 win over Colombia in May 2008

Following Norwich's relegation at the end of the 2008/9 season, Was was linked with a move to Crystal Palace. He remained at Carrow Road, and played an integral role in the Championship title win scoring 14 goals in 42 appearances.

On 8th January 2011, Hoolahan signed a new contract with City that would keep him at the club until 2014. In April 2011, he was named in the PFA Championship Team of the Year.

Norwich won a second promotion, moving up to the Premiership, on 2nd May 2011 with a 1-0 win at Portsmouth with Wes playing a key role (44 appearances, 10 goals) in the Canaries' promotion challenge.

Hoolahan scored Norwich's first goal in the 2011/12 Premier League campaign, equalising to give Norwich a 1-1 draw at Wigan on 13th August 2011. Impressive form in Norwich's opening start to the 2011/12 premier League season saw Hoolahan linked with a recall to the Irish squad, with Irish coach Marco Tardelli revealing that that Norwich City trio Wes Hoolahan, Anthony Pilkington and Marc Tierney are firmly on his international radar ahead of the Euro 2012 finals. The former World Cup winner, who was at Carrow Road to see the Canaries take on Arsenal, admitted he and Ireland manager Giovanni Trapattoni were weighing up all their options with regards to their final 23-man Euro2012 squad.

At the end of February 2012, Wes was voted into Norwich City's Hall of Fame

Hoolahan finished the 2011/12 season with 37 appearances and five goals as Norwich finished 12th in the Premier League.

Wes was recalled to the Ireland squad in August 2012 but had to withdraw through injury.

In December 2012, Wes signed an improved contract which would keep him at Norwich until June 2015.

Hoolahan scored his first goal for Ireland on 6th February 2012 in a 2-0 win over Poland, scoring in the 76th minute after coming on as substitute for Shane Long on 62 minutes.

In January 2014, Wes was the subject of media speculation that former Norwich manage Paul Lambert had made a £750,000 bid for him to join Aston Villa and that Wes had submitted a transfer request. This was denied by the club. Hoolahan submitted a formal transfer request on 21st January 2014. City released a brief statement on Tuesday evening confirming the 31-year-old Irish international’s wishes, while at the same time reiterating their belief that Hoolahan will be going nowhere during the January transfer window. But Hoolahan issued his own statement shortly after, acknowledging his desire to leave the Canaries following more than five and a half years at the club.

“Following a meeting with chief executive (David McNally), I felt I had no option but to hand in a transfer request,” said Hoolahan. “I have noted that request has been turned down. However, I believe it is in the best interest of Norwich, for whom I have the greatest respect, and myself that I am allowed to move on and play my football elsewhere.”

Aston Villa subsequently made a second bid which the Canaries rejected whilst it was reported on 31st January 2014 that West Brom had made an approach to take Hoolahan on loan until the end of the 2013/14 season. Newcastle were also reported to be interested.

He made 18 appearances, scoring once in the 2013/14 season in which Norwich were relegated from the Premier League. At the end of the season, he submitted another transfer request. Hoolahan eventually signed a new contract in August 2014 prior to the start of the new season.

On Transfer Deadline Day (2nd February 2015), Hoolahan was strongly linked with a move to Celtic but it did not materialise.

In an interview with the Irish Independent at the end of March 2015, Hoolahan revealed that he had trialed with Ipswich, Sunderland, Leicester and Millwall before joining Livingston.

On 20th April 2015, Hoolahan was named in the Football League Team of the Decade at their tenth Football League Annual Awards ceremony.

Hoolahan made 40 appearances in 2014/15 including playing in the 2-0 Championship Play-off final victory over Middlesbrough on 25th May 2015. He scored five goals including a penalty against Ipswich in the play-off semi finals.

Hoolahan was part of the Ireland squad that qualified for the Euro 2016 finals in November 2015.

Hoolahan made 30 appearances for City in 2015/16, scoring four goals, as the Canaries were relegated from the Premier League. On 31st May 2016, he was selected for the Irish squad who would completed in the European Championship in France in June/July 2016.

On 10th June 2016, Norwich announched that Wes had signed a contract extension until 2017. Three days later, he scored Ireland's opening goal in the European Championships in a game that finished 1-1 with Sweden.

Wes made 33 appearances in 2016/17 (scoring seven goals) and taking him to over 300 appearances for the club

Hoolahan played in the 5-1 defeat to Denmark on 14th November 2017 in a World Cup play-off qualifier which ended Irish hopes of reaching Russia 2018. Hoolahan came on at half-time to win his 42nd cap. In February 2018, he announced his international retirement.

Norwich announced at the end of April 2018 that they would not be renewing Wes' contract. His final and 352nd game for Norwich was the 2-1 home win against Leeds on 28th April 2018 in which Wes scored City's first goal and set up Josh Murphy for the winner. Former colleagues gave the following testimonials:

Russell Martin:“A true legend and one of the best ever to wear the shirt for @norwichcityfc. An absolute honour and a pleasure to play alongside the little magician for so long. Some footballer. Some man."
Grant Holt: "“Little Wessi is leaving Norwich, the greatest player Norwich have had in my opinion.10 derby days and no defeats, top that.”
Elliott Bennett: “I’m sure Wessi will get the send off he deservesGreat man, humble and what a player. Pleasure to have shared a dressing room with him.”
Nathan Redmond: “What an honour it was to watch, learn and play with you my friend. The legend, the magician, the GOAT! All the best on your next venture from a massive 10 years served @NorwichCityFC! #Wessi #LivingLegend.”
Darren Huckerby: "Will rightly be remembered as a all time #Ncfc great"

On 14th September 2018, Hoolahan signed for West Bromwich Albion on a short-term deal. Four days later Hoolahan made his Albion debut in a 4–2 win against Bristol City as a 74th minute substitute. Hoolahan was released at the end of the 2018/19 season having failed to start a Championship game for the Baggies. Former England international Gareth Barry, Scotland midfielder James Morrison were also not offered deals, but have been told they could stay if the incoming head coach wants them. Goalkeeper Boaz Myhill and defender Tyrone Mears are the others not on the retained list.

On 19th June 2019, it was reported that Hoolahan would train with Cambridge United during the 2019 pre-season whilst considering a contract offer from the League Two side. He played for them on trial, playing against Leicester on 23rd July 2019. On 31st July 2019, it was reported that Hoolahan had rejected a contract with Cambridge to explore the possibility of playing in Australia with the Newcastle Jets named as potential destination. He completed his move to the Jets on 8th August 2019, signing a one year contract with the Hyundai A-League club from the Hunter Valley. He said “It’s always been a dream of mine to play abroad and I’m delighted that I’ll be playing in Newcastle this season, There are some quality players throughout the league and I’m looking forward to testing myself in a new environment. I’m really excited to be coming to Australia, it’s an entirely new challenge for me and I can’t wait to get started.”

In December 2019, Hoolahan was named in the English Football League's Championship side of the Decade, chosen by over 60,000 votes on social media.

On 26th June 2020 Hoolahan left the Newcastle Jets as play had been suspended in March due to the Covid-19 pandemic and he chose to return to family in Ireland. It was reported that he was not returning to Newcastle when the season restarted on 16th July 2020 but that it was possible he could return in December 2020 for the new season. He had played just six games for the Jets due to suffering an ankle injury on his debut which required surgery.

On 28th July 2020 Hoolahan signed a one year contract with Cambridge United. He said “It’s a great move to a really good club and I’m delighted to sign for Cambridge United. I was obviously on trial here for four weeks last year and I enjoyed my time. I knew what the training ground was like, what the boys are all about and that all factored into my decision to sign. I’m grateful for the opportunity and hopefully I can reward the likes of Ben Strang (head of football) and Mark Bonner (head coach) who have kept this option open for me, during the forthcoming season. I’ve met with Mark last week and he’s said some great things, he’s passionate about the game and going forward it’s clear he wants the club to succeed. I’ll enjoy working with him."

Hoolahan played an instrumental role as Cambridge finished second in League Two in 2020/21 and was named in the divisional team of the season. He played 30 times the following season as they finished 14th in League One. He was released at the end of the season,

In February 2024 Hoolahan was one of four shock signings by 11th tier Doncaster City who play in the Abacus Lighting Central Midlands Alliance League. The others being Charlie Mulgrew, Ross McCormack and Scott McLaughlin. He made his debut on 17th February in an Abacus Lighting Central Midlands Alliance League clash at home to Dearne and District.