Lockyer currently plays in the five-eighth position, having moved there from his previous position of fullback in 2004. Upon switching positions, Lockyer endured heavy criticism, but responded in 2006 with arguably his finest ever season, becoming the first person since Allan Langer (a former teammate) to captain winning teams in the National Rugby League premiership, the State of Origin series, and the Tri-Nations series all in the same year. Lockyer also became only the second player to have won the golden boot award twice.
In 1998 Lockyer became the regular Queensland Maroons' fullback for the State of Origin and also made his debut for the Kangaroos. He was again top point-scorer for Brisbane that year, breaking the club record for most points in a season, and again played at fullback in the Broncos' premiership-winning team at the end of the 1998 season.
In 2000, Lockyer won another premiership with Brisbane and was awarded the Clive Churchill Medal for best and fairest player on the field in the Broncos' Grand Final win. Also that year he received the Australian Sports Medal for his contribution to Australia's international standing in the sport of rugby league and played in the 2000 Rugby League World Cup-winning Kangaroos side.
Following Queensland skipper Gorden Tallis' season-ending neck injury before the second game of the 2001 State of Origin series, the Maroons' captaincy was handed to Lockyer. In the third and deciding game of the series, Lockyer was named man-of-the-match, scoring two tries and kicking four goals to help Queensland to victory.
Along with Lote Tuqiri and Chris Walker, Lockyer was the Broncos' top try-scorer in the 2002 season and won the club's player of the year award for both the 2002 and 2003 seasons. He also won his first RLIF Golden Boot Award for the world's best international rugby league player in 2003. In addition, with the retirement of Tallis from representative football that year, Lockyer became the captain of both the Queensland and Australian teams.
Lockyer gained some negative media attention at the start of the 2004 season when he made a careless joke about the Bulldogs gang rape allegation at a Queensland sports function. Being the Australian captain, Lockyer was rebuked by national officials and quickly apologised for the comment.
With Gorden Tallis' retirement at the end of the previous season, the Broncos' captaincy was passed onto Darren Lockyer in 2005. In 2005 Lockyer was also the Broncos' top point-scorer, however experienced rugby league commentators continued questioning Lockyer's value as a five-eighth during representative matches.
However, after the ANZAC Test, in which Lockyer scored two tries in Australia's 50-12 defeat of New Zealand, the critics eased off. Lockyer's performances in the five-eighth position improved greatly in the weeks leading up to Origin, resulting in his selection as five-eighth and Captain for Origin 1.
Lockyer underwent further criticism when the Maroons lost to the Blues 17-16 after a poor first half. His position was again debated, but strong performances against the Bulldogs and the Warriors resulted in his retention in the Queensland side. Queensland then made an impressive comeback in Origin 2, thumping the Blues 30-6 while Lockyer received the Man of the Match award. He was then responsible for sealing the series victory for Queensland in the deciding match. With Queensland down 14-10 with 5 minutes remaining, Lockyer intercepted a pass from NSW player Brett Hodgson and scored the match-winning try. It was Queensland's first outright series victory since 2001 and also stopped New South Wales' from achieving their 4th consecutive Origin series win. After the match, Lockyer received the Wally Lewis Medal for player of the series.
Immediately after Queensland's State of Origin success, the Broncos entered a 5-game losing streak, but bounced back to comfortably win their final three premiership games of the season. Despite losing to the St George Illawarra Dragons in the first week of the finals, the Broncos rebounded to defeat the Newcastle Knights 50-6. They then won the preliminary final against the Bulldogs 37-20 after trailing 20-6 at half-time, with Lockyer named man of the match. He then steered his team to win the 2006 Grand Final 15-8, setting up both tries and then kicking a winning field goal in the 73rd minute. This was Lockyer's fourth premiership (first as captain), and the Broncos' sixth. Lockyer was also the Broncos' top try-scorer (together with Tame Tupou) for the 2006 season.
Lockyer then captained Australia to an extra-time victory in the Tri-nations final against New Zealand, scoring the match-winning try in Australia's 16-12 victory. In the process, he became the top try-scorer in Tri-Nations history with a tally of 9 tries.
In the week leading to the final, Lockyer won the RLIF Golden Boot Award for the second time. Lockyer was also named Dally M five-eighth and representative player of the year, the Broncos' best back, and people's choice player of the year, as well as being a finalist in the Queensland Sports Star of the Year award.
In the Round 18 match against North Queensland, Lockyer ruptured his anterior cruciate ligament, with the severity of the injury forcing him out for the rest of the 2007 season. He was scheduled to return for the March pre season games in 2008.
Lockyer is contracted to the Broncos until the end of 2009.
Lockyer has been strongly linked with a move to the European Super League at the conclusion of the 2008 NRL season. Darren Lockyer has admitted he would like to play in Super League before he retires. He has been linked with a move to Bradford Bulls and Catalans Dragons. Lockyer stated of his desire to move in the future, "Not just playing here but living in a different culture - it's appealing." He admits he had his appetite for a stint in Britain whetted by the Challenge Cup final and that he would be open to offers from Super League clubs for his swansong. It has since been confirmed by his manager George Mimis that up to six Super League clubs are hoping to lure Darren Lockyer to England, with London based Harlequins Rugby League said to be early front-runners for the Australian captain's signature. He has also been linked with Hull KR.
A troublesome knee injury resulted in surgery which kept Lockyer off the field for much of the first half of the 2008 season.
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