In October 2000, Whelan played for the Republic of Ireland under-16 national team in a qualifying tournament in Riga for the 2001 UEFA European Under-16 Championship where he came up against Andrés Iniesta. He represented the Republic of Ireland Under-20 team at the 2003 FIFA World Youth Championship and has been capped 14 times by the Irish Under 21s, captaining the side on many of these occasions.

Whelan started his career with Manchester City joining from Irish feeder club Cherry Orchard in 2001. He made a solitary appearance in the UEFA Cup coming on as a substitute for Paul Bosvelt against Total Network Solutions in August 2003, before joining Bury on a one-month loan the following month. After appearing in the Republic of Ireland’s 2003 FIFA World Youth Championship campaign in November and December, he returned to Bury on another one-month loan on 24 December 2003. In total Whelan played 15 times on loan at Bury and caught the attentions of Sheffield Wednesday manager Chris Turner.

In July 2006, Whelan was placed on the transfer list by Sturrock following increased competition for places in the Wednesday midfield after the arrival of Wade Small, Kenny Lunt and Yoann Folly. He was subsequently removed from the transfer list by the following manager, Brian Laws. Whelan repaid the faith shown in him with seven goals. He then went on to win a number of player of the year awards for the club’s 2006–07 season. His performances led to manager Laws entering into contract negotiations with Whelan. Sheffield Wednesday rejected bids for Whelan from both Burnley and Plymouth Argyle in January 2008. However, a £500,000 bid from Stoke City was accepted on transfer deadline day.

His first cap for the Republic of Ireland national B team came on 20 November 2007 against Scotland. Whelan made his debut for the senior team against Serbia in May 2008 and scored his first international goal against Georgia in Mainz, Germany on 6 September 2008. Since the appointment of Giovanni Trapattoni, Whelan became a key member of the squad and made 11 straight appearances despite previously being considered an “also-ran”. He scored his second goal for Ireland against Italy with a spectacular strike from almost 25 yards on 10 October 2009 in a 2–2 draw. Whelan started the matches in both legs against France as Ireland were controversially knocked out 2–1 on aggregate after extra-time.

Whelan joined Stoke City on 30 January 2008 for £500,000 signing a three and a half-year contract. He made his first Stoke City appearance in a Championship match against Cardiff City on 2 February 2008 when he came on as a substitute in the 82nd minute for Mamady Sidibé. Whelan made his first Stoke City league start the following match in a 4–2 victory against Wolverhampton Wanderers. He scored his first goal for Stoke in a 2–1 home defeat to Crystal Palace on 7 April 2008. Whelan played 14 times for Stoke City in the 2007–08 season as Stoke finished 2nd and were promoted to the Premier League.

Whelan started the club’s first match in the Premier League against Bolton Wanderers. Whelan did not have a good match and as a result he did not feature much in the first team, only playing in League Cup fixtures and even reserve matches. Despite this setback, Whelan was still a regular in the Irish national team. In December 2008 Whelan was being linked with a move away from the Britannia Stadium but he revealed that he wanted to stay. Whelan did manage to force his way back into the first team and he became an important player in Stoke’s successful fight for survival. Whelan scored a last minute equaliser away against Aston Villa on 1 March. Whelan signed a new four-year contract with Stoke on 15 September 2009. He scored his first goal of the 2009–10 season against Tottenham Hotspur which earned Stoke a 1–0 victory. He also went on to score against Manchester City in a 1–1 draw with Whelan beating fellow Irish international Shay Given. Arsenal player Aaron Ramsey praised Whelan for his support after Ramsey’s suffered a leg break in a match between Stoke and Arsenal.

He made his 100th appearance for Stoke in a 2–0 win over Everton on 1 January 2011. After drifting in and out the starting eleven for most of the 2010–11 season Whelan made a return in March and has played a key role in Stoke’s run to their first FA Cup Final. Whelan reached a century of league appearances for the club on 8 May 2011 against Arsenal. Whelan played in the 2011 FA Cup Final as Stoke lost 1–0 to his old club Manchester City.

Whelan scored a rare goal for Stoke against FC Thun in the UEFA Europa League in August 2011. In a match against Bolton Wanderers referee Howard Webb awarded an indirect free-kick inside the penalty area for a back-pass against Whelan after two minutes. Kevin Davies scored from the quickly-taken restart to put Bolton ahead. Stoke chairman Peter Coates criticised Webb’s controversial decision to penalise Whelan. He scored his first league goal for more than 18 months against Blackburn Rovers in November 2011. In January 2012, manager Tony Pulis confirmed that he wanted Whelan to sign a new contract stating “Every time you ask Glenn to step up to that next level, he does it. He’s a good lad, very single-minded. He’s got that Celtic blood in him and the determination to prove people wrong – including myself at times”. Whelan signed a new three-and-a-half-year contract on 11 January 2012 and said “I am loving life at the moment and things are going really well, so I am absolutely delighted to commit my long-term future to the club”.

In March 2012, Whelan made his 37th international appearance for the Republic of Ireland, with all of his caps coming whilst at Stoke he surpassed Gordon Banks’ record becoming Stoke’s most capped player. In the summer of 2012, Stoke signed midfielders Charlie Adam and Steven Nzonzi and Whelan’s place in the side came under threat but he ‘lifted his game’ and retained his place for 2012–13 season. He avoided a ban after a ‘two footed’ tacked on Manchester City’s Javi García in the FA Cup. Whelan played 34 times in 2012–13 as Stoke finished in 13th position. He ended the season on a sour note as he was involved in a dressing room bust-up with Kenwyne Jones.

Whelan won his 50th Irish cap on 14 August 2013 against Wales. He was branded a “terrible” player by RTÉ pundit and former Republic of Ireland international Eamon Dunphy in the aftermath of a poor performance in a 2014 FIFA World Cup qualifying match against Sweden. Whelan hit back at Dunphy stating that he is nothing more than a “media bully”.

Whelan retained his place in the side at the start of the 2014–15 season before he was ruled out of six weeks suffered a fractured leg whilst on international duty with Ireland in October 2014. He returned to the side in December 2014 after successfully recovering from his injury. Whelan signed a two-year contract extension in January 2015. In February 2015, Following an injury to captain Ryan Shawcross, Whelan acted as stand-in captain and after a woeful 4–1 defeat against Blackburn Rovers in the FA Cup Whelan had a dressing room rant at his teammates. Whelan played 30 times for Stoke in 2014–15 as the Potters finished in 9th position for a second season running and they ended the campaign with a 6–1 victory against Liverpool. His performances during the campaign earn him the praise of teammates Adam and Shawcross who both described Whelan as the teams ‘unsung-hero’.

Whelan was again a key figure under Hughes in 2015–16, making 42 appearances as Stoke again finished in 9th position. He also filled in as stand-in captain during the season due to injury to Ryan Shawcross. He made his 300th appearance for Stoke on 12 March 2016 against Southampton, however he was not to be on the winning team as Stoke lost 2–1 at home. At the end of the campaign, Whelan admitted that he was disappointed that the team did not finish higher in the table.

Prior to the start of the 2016–17 season, Whelan signed a one-year contract extension in July 2016, which ties him to Stoke until the summer of 2018. Whelan played 31 times in 2016–17, as Stoke finished in 13th position. Whelan gave an honest assessment of Stoke’s campaign following a 2–2 away at AFC Bournemouth on 6 May 2017. “We’re disappointed, being twice up away from home especially to a team like Bournemouth and giving away two sloppy goals pretty much sums up our season I think”.

Whelan joined Aston Villa on 20 July 2017 on a two-year contract for a fee of £1 million. He scored his first goal for Aston Villa in a 4–2 win at Sheffield Wednesday on 24 February 2018. Whelan played 35 times in 2017–18 helping Villa reach the 2018 EFL Championship play-off Final where they lost 1–0 to Fulham. He made 38 appearances in 2018–19 as Villa again managed to reach the play-off final this time beating Derby County 2–1. At the end of the campaign Whelan’s contract was not renewed by Dean Smith.

On 14 August 2019, Whelan joined Scottish Premiership side Heart of Midlothian on a one-year contract. He left the club in January 2020, after new manager Daniel Stendel had dropped him from the team. Whelan subsequently criticised Hearts, saying that he felt like he had been “thrown under a bus” by the club and described the way they handled his departure as “amateurish”. Conversely, it was later revealed that Whelan had made little or no effort to become involved in the club, and – in the words of journalist Tom English – ‘club, players and fans alike were unconvinced by the level of commitment the Ireland international showed towards the club … [and] not one person is sorry to see him go. Not one.

Whelan earned his 90th cap against Switzerland in October 2019 making him the ninth most capped Irish player of all time.

Whelan signed a short-term deal with League One club Fleetwood Town on 24 January 2020, joining until the end of the season.