Crocker has led the Premier League club's youth setup for the last seven years, overseeing the emergence of talents such as Gareth Bale, Alex Oxlade-Chamberlain and Luke Shaw in that time.
And that impressive track record has now earned him a job as head of coach and player development with the English football governing body.
"Matt will leave us with the best wishes of everybody associated with the club," Southampton chairman Nicola Cortese said in a statement.
"He has given Southampton seven years of hard work and dedication, and played an important part in developing the academy that we have today.
"Although we are sad to lose a talented member of staff, it is an honour to see the work of a Southampton employee recognised by the FA. We are ranked as the best academy for producing players for the English national teams, so it is no surprise that they have turned to Matt for this vital role.
"Matt will be hard to replace, but we expect serious interest from exceptional candidates who will be desperate to work for an Academy with a reputation such as ours."
Southampton lost both Theo Walcott and Oxlade-Chamberlain to Arsenal in recent years, while Bale left the club in order to link up with Tottenham.
However, Shaw last week extended his stay at St Mary's by signing a new five-year contract on his 18th birthday.