Popovic started his managing career in 2008 with Sydney FC. After a brief stint as assistant at Crystal Palace he was chosen as the inaugural manager of Western Sydney Wanderers at the start of the 2012–13 season.
Tony Popovic signed for Crystal Palace on a free transfer in August 2001 from Sanfrecce Hiroshima. He became an integral part of the Palace defence, eventually becoming club captain. He played more than 120 matches for Crystal Palace. In his last season he played for Crystal Palace in 21 Premier League matches. In total he made more than 120 appearances for the club.
Popovic's contract with Palace expired at the end of June 2006, and he decided against accepting the club's offer of a new contract. He instead moved to Qatar club, Al-Arabi.
In 2007, with the growth of the A-League and slight homesickness, Popovic moved to Sydney FC, signing a two-year deal, with coach Branko Čulina also announcing him the club's captain. Popovic scored his first goal on 28 October 2007 from a corner to beat the Mariners 3–2 in front of his home crowd of 17,850.
Popovic announced his retirement on 11 November 2008 after nearly 20 years as a professional footballer.
Popovic competed at the 1992 Summer Olympics in Barcelona for the Australian U-23 team. He began his full international career in 1995 with the Australian national team. Over the next eleven years Popovic made 58 appearances for the Socceroos, scoring 8 goals.
The highlight of Popovic's career came in 2006 when the Australian national team qualified for the FIFA World Cup under the management of Guus Hiddink. He took part in both legs in the qualifying match against Uruguay. Being replaced in the first half of the second leg due to injury by Harry Kewell. The tall defender was named in the competing squad and made his World Cup debut against Brazil on 18 June. He suffered a calf injury 40 minutes into the game and was replaced by Marco Bresciano for the second half. His injury ruled him out of Australia's last match in the group stage, against Croatia, and their second round loss against eventual winners, Italy.
On 4 October 2006 Tony Popovic announced his retirement from the Socceroos.
His final game was a friendly against Paraguay that month. He scored his eighth international goal, from a Mark Bresciano free kick, in his final minute on field to put Australia ahead, 1–0 in a game that finished 1–1.
After retiring, Popovic moved into an assistant coach's role with Sydney FC, where he remained until February 2011, when he returned to England and to Crystal Palace as first team coach, after former team-mate Dougie Freedman was appointed manager.
On 17 May 2012, Popovic was announced as inaugural manager of A-League club Western Sydney Wanderers. He joined the club on a four seasons deal after requesting to be released from the final year of his contracted role as assistant manager of Crystal Palace. In Wanderers' first season, Popovic was named A-League Coach of the Year after finishing first in the league. In the 2013/14 season Popovic led Wanderers to the 2014 AFC Champions League Final in the clubs first attempt in the competition. They defeated Al-Hilal in the final, becoming the first Australian team to win the tournament. As a result of this achievement, Popovic was named as the 2014 AFC Coach of the Year. With poor recruiting, the loss of assistant coach Ante Milicic, and a grueling schedule of matches, the 2014/15 season saw Popovic's team finish ninth in the league and eliminated from the group stage of the 2015 AFC Champions League. Despite an unfavorable season Popovic signed new three-season deal with Western Sydney Wanderers, which would keep him at the club helm until 2018.