Starting in 1989 at Sydney United he went on to play for Sanfrecce Hiroshima of Japan and Premier League side Crystal Palace, among other clubs.

He holds the record of coaching the most A-League Grand Final losses with 5 to the end of the 2023/2024 season He is the father of Kristian and Gabriel Popovic, both of whom are also professional footballers.

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 Culina also announcing him the club's captain.

The highlight of Popovic's career came in 2006 when the Australian national team qualified for the 2006 FIFA World Cup under the management of Guus Hiddink.

The tall defender was named in the competing squad and made his World Cup debut against Brazil on 18 June.

[6] 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.

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.

[11] 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.

[14] On 1 October 2017, Popovic made a shock announcement that he had resigned from Western Sydney Wanderers to coach Turkish Süper Lig club Karabükspor.

On 26 August 2020, shortly after coaching Perth to a 2–0 loss to Sydney FC in the A-League semi finals, Popovic activated a contractual clause allowing him to leave the club for a European team, after signing with Greek Super League side Xanthi FC, that was bought by Greek-Australian business tycoon Bill Papas.

Goalkeeping coach Zeljko Kalac stated later that Popovic was sabotaged and fired due to the owners wanting more control over decisions.

[21] Popovic had early success, bringing the club back to the top of the A-League table after eight games and winning the 2021 FFA Cup on 5 February 2022.