Hoolahan played as a schoolboy for Belvedere. He also played futsal with Belvedere. He started his senior career at Shelbourne where he won three League of Ireland Premier Division championships and excelled during their run in the 2004–05 UEFA Champions League qualifying rounds. He was the PFAI Young Player of the Year in the 2002–03 season. He then had a brief spell at Livingston.
On 21 July 2006, Hoolahan joined Blackpool on a season-long loan. He scored his first goal for the club on 30 September 2006, a penalty in a 3–0 win over Leyton Orient at Bloomfield Road. On 15 December 2006, he scored a goal and was sent off in a 3–1 win at Scunthorpe United.
In June 2007, Hoolahan signed a two-year contract with Blackpool. Livingston, however, refused to sign the documentation sanctioning the move, stating that Blackpool had repeatedly breached the terms of the loan agreement. Blackpool denied any such default and referred the matter to the Football Association. With Livingston being backed by the Scottish Football Association the matter was passed to FIFA for a decision to be made on the player's future. On 10 August 2007, FIFA ruled in Blackpool's favour, thus confirming Hoolahan as a Blackpool player.
On 26 June 2008, Norwich City confirmed the deal to bring Hoolahan on a three-year player-plus-cash deal. Norwich reserve team keeper, Matthew Gilks, moved in the opposite direction along with an undisclosed amount of money. Hoolahan was handed squad number 14, which he has kept in his time at Norwich. His first goal for the club finally came when he opened the scoring in a 4–0 win over Barnsley at Carrow Road on 17 January 2009. An injury sustained on 14 March, whilst playing against Plymouth Argyle, kept him out for the rest of the season as Norwich were ultimately relegated to League One.
In 2009–10, under new manager Paul Lambert, Hoolahan was utilised in a role behind the strikers in a midfield diamond formation as opposed to on the wing. This saw a higher personal goal return for Hoolahan as he scored 13 times (including four penalties) in all competitions before the new year.
In the 2010–11 season, Hoolahan scored his first two goals of the season against Leicester City, scoring a penalty and a 30-yard half-volley shot. Like the previous season, Hoolahan was utilised at the tip of the diamond formation. Hoolahan continued his good form, with a goal against Bristol City, making it three goals in two matches for him. On 28 December 2010, Hoolahan scored his first hat-trick for Norwich City in a 4–2 win over Sheffield United after coming on as a substitute.
Hoolahan signed a new three-and-a-half-year deal with the club in January 2011, committing his future to Norwich until 2014.
During pre-season before the 2011–12 Premier League campaign, Hoolahan was given the captain's armband when club captain Grant Holt and vice-captain Russell Martin were not playing. He led out the Canaries for the first time in the friendly fixture against Southend United at Roots Hall. He scored his first Premier League goal in Norwich City's opening day 1–1 draw against Wigan Athletic on 13 August 2011. Hoolahan led the Norwich team out as captain for their first Premier League win of the season, a 2–1 away victory against Bolton Wanderers on 17 September 2011, being given the armband ahead of the previous season's regular vice-captain Russell Martin who was also in the team. He was inducted into Norwich City's Hall of Fame on 20 March 2012.
On 15 December 2012, it was announced Hoolahan had signed a new deal with Norwich City worth a reported £40,000 per week, keeping him at the club until 2015.
In January 2014, Hoolahan was the subject of transfer speculation from Aston Villa who reportedly had a bid of £1 million rejected. A few days after this reported bid, Hoolahan put in a transfer request which was turned down by the club. On 7 March, Hoolahan scored the opening goal against Villa in a 4–1 defeat, and executed a muted celebration.
In August 2014, Hoolahan signed a new contract to keep him at the club until the end of the 2016–17 season.
On 19 April 2015, Hoolahan was selected in the Football Manager Team of the Decade at the Football League Awards.
On 1 August 2016, Hoolahan agreed a new contract to keep him at Norwich City until 2018.
On 7 May 2017, Hoolahan was announced as Norwich City's Player of the Season for 2016–17. On the last game of the 2016–17 season, Hoolahan scored two goals and one assist against QPR on the 7th of May 2017.
Hoolahan was first capped at under-21 level for the Republic of Ireland. While at Shelbourne, he was an unused substitute in Don Givens' first game in charge of the Republic of Ireland, a 0–0 draw against Greece in November 2002.
Hoolahan was named in the Republic of Ireland "B" squad on 8 November 2007, for the match against Scotland on 20 November at the Excelsior Stadium in Airdrie. Hoolahan played in the match, which ended in a 1–1 draw.
In April 2008, Giovanni Trapattoni included Hoolahan in his preliminary 40-man squad for the friendly matches against Serbia on 24 May and Colombia on 29 May. On 13 May it was confirmed that Hoolahan had made the 28-man squad and that he would be joining a training camp in Portugal on 15 May in preparation for the matches. He came on as a 70th-minute substitute in a practice match which the Irish team drew 1–1 with Portuguese Liga de Honra club side Portimonense. He was an unused substitute in Ireland's 1–1 draw with Serbia at Croke Park in Dublin. On 29 May, he came on as a second-half substitute in the 1–0 win over Colombia held in England at Craven Cottage.
On 10 August 2012, Hoolahan was recalled to the Republic of Ireland squad for the 15 August friendly international against Serbia in Belgrade. However, he was unable to accept the call due to an Achilles tendon injury.
On 31 October 2012, Hoolahan was called up to the Republic of Ireland squad for the 14 November friendly international against Greece in Dublin. He came on at half-time in the 1–0 defeat replacing Robbie Brady and earning his second cap for the Republic of Ireland. On 6 February 2013, Hoolahan scored his first goal for Ireland in a 2–0 defeat of Poland in a friendly in Dublin.
After being rarely used during the Trappatoni era, Hoolahan was selected for Martin O'Neill's first game as Irish manager against Latvia. Ireland won the game 3–0. Hoolahan has flourished under O'Neill, picking up the Man of the Match awards against Serbia and Turkey. Former Norwich City teammate Anthony Pilkington has called for O'Neill to build the team around Hoolahan for the Euro 2016 qualifiers.
On 11 October 2014, despite not being used in the first qualifying game against Georgia, O'Neill restored Hoolahan to the starting 11 against the minnows Gibraltar. Hoolahan was heavily involved in the game with his sublime ball finding Aiden McGeady who crossed to Robbie Keane who made it 1–0. He then assisted Keane for the second goal and won the penalty which Keane converted to make it 3–0. Hoolahan scored the 7th goal which rounded off the rout and he also picked up the Man of the Match award for his brilliant performance.
On 29 March 2015, Hoolahan started Ireland's crucial Euro 2016 qualifier against Poland in the Aviva Stadium. The game finished 1–1 with Hoolahan getting the assist for Shane Long's injury time equaliser. Hoolahan picked up the Man of the Match award with Johnny Giles and Eamon Dunphy praising his performance.
Hoolahan scored the first goal for Ireland at UEFA Euro 2016 in Ireland's opening group-stage match against Sweden. He earned the Man of the Match award for his display in an eventual 1–1 draw. On 22 June 2016, Hoolahan came on as a substitute for James McCarthy in the 77th minute in Ireland's final Euro 2016 group game against Italy. He provided the assist for Robbie Brady's 85th-minute winner to send the Republic of Ireland through to the last 16. Moments prior to the goal, Hoolahan had missed a great one-on-one chance.As of match played 12 November 2016. Republic of Ireland score listed first, score column indicates score after each Hoolahan goal.
As of match played 9 September 2017
As of match played 10 June 2017
League of Ireland (3): 2002, 2003, 2004
League One Play-offs (1): 2007
Championship Play-offs (1): 2015
Championship (1): 2010–11 (Runner-up)
League One (1): 2009–10
Football League Team of the Decade (1): 2015
Football League One PFA Team of the Year (2): 2006–07 2009–10
Football League Championship PFA Team of the Year (1): 2010–11
PFAI Young Player of the Year (1): 2002–03
Norwich City Player of the Season: 2016–17