The MLS club confirmed his departure late on Saturday evening, with officials insisting that it was a “mutual” agreement.
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A statement from DC United CEO and Co-Chairman Jason Levien read: “We have spoken with Wayne and agreed it is best for us to part ways at this time.
“This decision creates the avenue for our next General Manager to have the full opportunity to impart a new philosophy and structure onto our sporting operations, which begins with the critical identification of a Head Coach who will best align with this.
“We are grateful to Wayne Rooney for all he has done for our club and for soccer in the Nation’s Capital, first as a D.C. United player and captain and most recently as our coach.
“He remains an important part of the D.C. United family and a valued and cherished friend.”
Addressing his departure, Rooney said: “It’s the right time. I’ve done everything I can to get this club into the playoffs. It’s not a single thing that’s happened. It’s about timing.
“What lies ahead, I don’t know. I’ve seen a lot of reports in the media. I’m going back with nothing lined up.”
Rooney returned to DC United in July 2022 after leaving Derby County.
He was in charge of the Washington-based side for 52 games, racking up just 13 wins and 26 defeats.
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The Manchester United legend is now set to return to England, but he is yet to find a new job.
Rooney has been heavily linked with a move to Birmingham City, with current manager John Eustace tipped for the vacant Rangers position.
Blues co-owner and NFL icon Tom Brady has been in constant contact with the former striker in recent weeks over the job.
Brady believes Rooney will be able to attract big players to St Andrew’s and eventually lead the club back to the Premier League.