The MLS welcomes Cushing where he will be assistant manager to newly appointed New York City FC manager, Ronny Deila.
Cushing joined the club in 2008 and since taking charge of Manchester City Women in 2013, the team has won six major trophies; one WSL title, three Continental Cups and two FA Cups.
The Citizens have finished top two in the WSL consecutively for the past four seasons and currently sit second just under Arsenal.
His final match will be on February 2 at home against Arsenal, who he beat during his first season as manager in the 2014 Continental Cup Final.
Following his departure, current assistant manager Alan Mahon will take charge as interim manager alongside Brian Eastick, former England men's Under-21s coach.
Time at City
City were only incorporated into the WSL in the 2014 campaign making Cushing the club's only women's manager thus far and has been an integral part of the club's growth and success.
Young players on the squad have praised Cushing given he is particularly known for bringing up young British talent in the squad such as the likes of Georgia Stanway, Lauren Hemp and Keira Walsh.
Cushing's five matches left in charge include City's Continental Cup quarterfinal against Sheffield United and the Manchester Derby for the fourth round of the FA Cup.
“Making the decision to leave MCWFC has been incredibly difficult given the fantastic players and staff that we have here and the incredible success that we have achieved together - it isn’t one that I have taken lightly," speaking to the Manchester City website.
“We’ve had an amazing six-and-a-half seasons and I have thoroughly enjoyed working with everybody – I will be extremely emotional to leave, but I’m very excited for my next role within the City Football Group.
“Linking up with New York City and Ronny (Deila) is a brilliant opportunity and I’m really looking forward to working in the MLS.”