Despite interest from several British sides Hawkins signed for Irish top flight club St Patrick's Athletic, where he linked up with fellow Bronze medallists from the FIFA World Youth Championships, Trevor Molloy and Thomas Morgan. Hawkins immediately earned a starting spot alongside Packie Lynch and their solid base helped St Pats win the championship in his first season. Hawkins played in the Champions Leaguepreliminary round against Celtic in 1998, in a 0–0 draw at Celtic Park. He was rewarded with the Players' Young Player of the Year Award. In November 1998 he was awarded the FAInational Leagueplayer of the year award. St Pats also won the league in Hawkins second season. During these years he would represent Ireland many times at Under 21 level. Hawkins was injured at the start of the 1999/2000 season and on his return was played in a deep midfield role. He was not comfortable there and his performance levels dropped remarkably. Towards the end of the season it was announced that he would not stay with St Pats, but join English Football Conference side Doncaster Rovers.
Doncaster Rovers
Hawkins was signed by Ian Snodin, but within weeks Snodin was sacked and replaced by Steve Wignall. Wignall did not rate Hawkins as highly as Snodin did, and initially Hawkins had to be content with only substitute appearances. He broke into the starting line up in November 2000 and remained there for the rest of the 2000/01 season. Hawkins had firmly established himself in the side during the first half of the 2001/02 season but was forced to leave the club, after Doncaster were forced to cut their playing squad down due to financial restrictions.
November 2001 saw Hawkins return to Ireland to play for Bohemians and he made his debut for the "Gypsies" against former club St. Pats on 30 November. In 2003 Hawkins won his third league winners medal as Bohemians won their second title in 3 years, though Hawkins was never a popular player in Dalymount Park due to consistent poor performances.
At the end of the 2004 season, Bohemians Dublin rivals Shelbourne signed 3 out-of-contract players from Bohemians; Hawkins, Glen Crowe, and Bobby Ryan. Hawkins won his fourth league title, and his first piece of silverware at Shelbourne, as they won their third title in 4 years in November 2006 defeating Bohemians 2–1 to clinch the top spot.
Coventry City
In January 2007 Hawkins made a free transfer back to Championship side Coventry City, the team where he signed his first professional contract. This time however Hawkins went on to make several very impressive appearances in his first season back, helping Coventry City stay clear of relegation. A troublesome Achilles injury restricted Hawkins to just a solitary start in his second season and with the arrival of new manager Chris Coleman he was deemed surplus to requirements and his contract was not renewed.
On 28 May 2008, it was revealed that Hawkins had become first signing by manager Micky Adams in his second spell as manager at League One Brighton, agreeing a two-year contract. Hawkins and Adams had previously worked together at Coventry. Hawkins was hugely popular with the Brighton faithful and assumed cult status at the club. Following the completion of his two-year contract, Hawkins was released by Brighton much to the dismay of many supporters.
Hawkins returned to Ireland in June 2010 when he signed for Sporting Fingal as he wanted to return home for family reasons. He was part of the team that bowed out the UEFA Europa league after losing 6–4 on aggregate to Marítimo. Hawkins found himself without a club three weeks before the start of the 2011 season after Sporting Fingal cancelled all their players contracts and later folded.
