Eagles made his first-team debut for Manchester United on 28th October 2003 as a second-half substitute for Kieran Richardson in an extra-time win away to Leeds United in the League Cup. He played once more that season, this time as a substitute for Cristiano Ronaldo as United lost 2–0 away to West Bromwich Albion in a League Cup Fourth Round tie.
On 21st December 2006, Eagles decided to take the option of returning to Manchester United after struggling to get many games at NEC Nijmegen. He only made 11 appearances for NEC, with the majority coming as a substitute. On 13th March 2007, Eagles featured in the second half for United in an exhibition match at Old Trafford against Marcello Lippi's Europe XI.
On 28th April 2007, Eagles scored his first senior goal for United in a 4–2 Premier League win over Everton. After coming on as a second half substitute, he scored a 93rd-minute goal to put the result beyond doubt and putting Manchester United five points clear in their race for the Premier League title. On 20th July 2007, during Manchester United's tour of Asia, he scored in a friendly match against FC Seoul. He also scored a spectacular 35-yard volley in a friendly match against Shenzhen FC four days later, bringing his total for the tour to three goals in five games. Eagles scored another pre-season goal the following year, netting United's equaliser against Kaizer Chiefs to earn a 1–1 draw. He also started in the pre-season game against Portsmouth in Nigeria, scoring United's opening goal.
Eagles was loaned to Watford on 21st January 2005, for whom he made 13 appearances and scored one goal (against Gillingham). He was also loaned to Sheffield Wednesday for the first half of the 2005–06 season. He scored his first goal for Sheffield Wednesday in their derby match against Leeds. He ended his loan spell with a total of three goals for Wednesday.
On 6th January 2006, Eagles was again loaned to Watford, making his debut against his future employers Bolton Wanderers in the FA Cup, with the Hornets going down 3–0. In his first league appearance for Watford against Stoke City, he scored the only goal of the match for Watford. His winning goal in the 1–0 away win at Brighton & Hove Albion on 18th February from 50 yards (almost the halfway line) – reminiscent of David Beckham's goal for Manchester United against Wimbledon a decade earlier – won him the club's goal of the season award. He also scored the first goal in the 4–1 thrashing away at Sheffield United, and David Unsworth was sent off for elbowing him. Having played almost every game for the Hornets since his loan move, Eagles was put on the bench for the play-off games.
On 31st August 2006, Eagles agreed to spend four months on loan at Dutch outfit NEC Nijmegen, in order to gain more experience.
On 29th July 2008, Eagles signed for Burnley on a three-year contract for an undisclosed fee. Manager Owen Coyle said, "He can play as a striker, or behind the striker or wide or as a central midfielder. He gives you a host of variations, but outwith that he's a talented footballer and that's what we want – young exciting talents to complement the quality we already have." Eagles made his league debut for Burnley on 9th August 2008 in a 4–1 loss to Sheffield Wednesday. On 27th September 2008, he scored his first goal for Burnley in a 3–1 victory over rivals Preston North End, scoring in the 95th minute.
In July 2010 the Clarets accepted a bid from Scottish champions Rangers to buy Eagles, but the player was unable to agree terms with the Scottish club and remained in England. He went on to score 15 goals in 48 appearances in his final season with Burnley.
On 29thuly 2011, Eagles and his Burnley team-mate Tyrone Mears joined Bolton Wanderers on three-year contract for a joint fee in the region of £3 million, linking up with their ex-manager Owen Coyle for a second time in their careers. He made his debut in a 4–0 away win at Queens Park Rangers on 13th August, where he created an assist for the second goal put in his own net by Danny Gabbidon. On 20th September, he scored his first goal for Bolton, from twenty five yards, in the League Cup Third Round 2–0 away win against Aston Villa. His first League goal for Bolton came on 15th October in a 3–1 win away to Wigan Athletic, where he also assisted the first goal, an own goal by Gary Caldwell. He also scored a brace in the 5–0 home win against Stoke City on 6th November. He found himself out of the starting line-up for a few games for a while due to Tuncay Şanlı being in form, but he came back to the starting line-up on 21st April 2012, where he scored in a 1–1 draw at home to Swansea City, and kept his place the following game, in the 2–1 away win to Aston Villa, where he provided the assist for the winning goal from David Ngog. At the end of the season, Bolton were relegated to the Championship.
Eagles became a key player for Bolton upon their return to the Championship and has been Bolton's top scorer from early in the season, scoring six times in the first few months against Derby County, Nottingham Forest, Hull City, Birmingham City, Millwall and Bristol City but despite being named Player of the Month by the fans for August, September and October of the new season, Bolton were in the bottom half of the table. Following Owen Coyle's sacking Dougie Freedman said that he wanted to base his team around Eagles. In 2013 Bolton's fortunes changed as they went from 20th to 6th within two months. However, come the end of the season they finished seventh meaning that they did not make the play-off places.
Eagles finished the season as Bolton's top goalscorer with twelve goals, and also created the most number of goals, with twelve assists. His form in April earned him a nomination for the Football League Championship Player of the Month.
At the end of the 2013-14 season he was released by the club along with Zat Knight, Tyrone Mears and Jay Lynch.
Luxury player imo, someone who can have a bit of magic from time to time to turn games BUT someone who doesn't put a shift in to help defend in front of the defence and as such it seems like we took to the field with ten men at times - nine when Petrov was playing as well.
Great vision once again by Coyle to sign Eagles (and Petrov too!).