In eleven seasons at Cardiff, Whittingham played 457 competitive matches and scored 96 goals, putting him seventh on the all-time appearances list and ninth among their goalscorers.

[6][7] Whittingham began playing football as a youth player with his local side Coventry City, joining the club at the age of seven.

[10][11] He was handed his first team debut on 21 April 2003 by manager Graham Taylor against Newcastle United, as a half-time substitution for Gareth Barry in a 1–1 away draw.

[14] After featuring regularly during the early stages of the campaign,[15] he scored his first senior goal against Wycombe Wanderers in the League Cup third round on 23 September 2003, during a 5–0 win at Adams Park.

[17] He finished the season having made 39 appearances in all competitions as a left-sided midfielder, including playing six times in the club's League Cup run where they reached the semi-final before losing to Bolton Wanderers,[15][18] a match in which Whittingham was later branded a "scapegoat" for his side's defeat.

[19][20] However, he gradually fell out of favour as the side struggled and, on 14 February 2005, Whittingham signed for Championship club Burnley on a one-month loan having not featured for Villa for nearly two months.

[23] Whittingham started all nine matches of his loan spell, seven in the league and two in the FA Cup,[19] before returning to Villa in late-March, despite Cotterill's hopes of extending the deal.

[24] Whittingham started three of Villa's opening four matches of the 2005–06 season,[25] but returned to the Championship on 15 September, joining Derby County on a three-month loan.

[25] On 11 January 2007, after making just five appearances for Villa since the end of his loan spell with Derby more than a year previously, Whittingham was transferred to Cardiff City for a reported fee of £350,000.

By mid-November Cardiff found themselves just above the relegation zone; this prompted a minor reshuffle from boss Dave Jones that involved Chris Gunter and Whittingham returning to the starting line-up.

He continued his scoring form with a brace against Watford[37] and goals against Crystal Palace[38] and Coventry City[39] followed by a hat-trick against Sheffield United.

[47] Whittingham scored a fantastic volley against Barnsley on 13 March, which ended up being voted Football League Goal of the Year award for 2011.

[51] Whittingham played a big role in Cardiff's centre midfield, producing many impressive performances and scoring several fine goals, including direct freekicks against Peterborough and Crystal Palace as well as a sublime chip from 35 yards away to Reading.

[54] Whittingham was part of all the matches in the League Cup campaign, which eventually saw Cardiff lose 3–2 on penalties to Liverpool in the final at Wembley Stadium.

[57] During the close season, more speculation about Whittingham's future in the Welsh capital arose, this time from Premier League club West Bromwich Albion.

After a drop in form, Whittingham was left out of the team towards the close of the season, but managed his eighth and final goal of the campaign with a last-minute penalty at home to Blackburn Rovers on 1 April.

Whittingham collected a winner's medal as Cardiff lifted the Championship trophy following April's home encounter with Bolton Wanderers.

[66][67] Whittingham scored twice in a 4–1 win over Brighton & Hove Albion and overtook John Toshack and Hughie Ferguson in the club's all-time leading scorers list in English league competitions.

[82] In March 2021, Pontypridd Coroner's Court recorded a verdict of accidental death, concluding that Whittingham was intoxicated and engaged in "horseplay" with friends before falling through a fire door and down a flight of stairs.

[83] In 2021, Whittingham's wife Amanda, brother James, sister Rachel and mother Sally founded a Registered Charity in his honour, named The PW7 Foundation.

[85] A tribute friendly was organised between Cardiff City and Aston Villa, which took place on 30 November 2022, during the break in both teams' respective leagues due to the 2022 FIFA World Cup.