Jamieson is due to play his 323rd and last ALM match in Saturday's decider against the Central Coast Mariners at CommBank Stadium, then join Rado Vidosic's coaching staff.
The 34-year-old is attempting to win his fifth trophy at City, with three premierships and a championship already to his name, all at the one club.
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"He's been a fantastic servant, leader, and gentleman," Vidosic said in a statement. "It has been an honour to coach him and to be part of his last season as a player.
"I'm really looking forward to him joining our A-League Men's coaching set up and helping him as he starts his new journey.
"He's going to continue be a very important part of the team and we will continue to learn from him through the leadership qualities that he will bring to the group."
Jamieson, capped by the Socceroos four times, has played at five ALM clubs, starting his career at Adelaide United while also having stints at Sydney FC, Perth Glory and the Western Sydney Wanderers. After a season at Swedish club IFK Goteborg, Jamieson joined City on a four-year deal.
He has cemented his reputation at City, where he drove the competitiveness that turned the club from underachievers into a powerhouse. That included scoring a penalty in their breakthrough Grand Final win in 2021.
His 161 appearances for City are a club record but this season he has been dislodged from left-back by breakout star and recent Socceroos debutant Jordan Bos.
Jamieson's post-playing career echoes that of fellow former City captain Patrick Kisnorbo, who moved into coaching after his playing days.
"It's fantastic to be able to offer Scott a pathway into coaching," City football director Michael Petrillo said. "He follows in the steps of Patrick Kisnorbo and is further proof that the club is committed to developing its talent and investing back into Australian football."