Killeen, 47, has been a one-club man on and off the pitch and has helped provide a steady stream of international players such as Stokes, Wood, Potts and Brydon Carse.
Now he is the one making the step up, inheriting the title of elite pace bowling coach.
Jon Lewis had previously filled that position, but took over as head coach of England Women late last year.
Killeen played over 350 times for Durham and finished his playing career in 2010 with 613 wickets across all formats.
He has previously been seconded to England's ODI squad, England Lions and the Under-19s and will focus on developing future prospects as well as working with the senior side.
"I'm delighted to be appointed elite pace bowling coach with the ECB and can't wait to get started with a new challenge," Killeen said.
"It's an exciting time to be joining the ECB, as there is a wealth of fast bowling talent and coaching around the country that I'm looking forward to working with in order to maintain England's strong contingent of pace bowlers in the future.
"I'd like to say a big thank you to everyone at Durham for their continued support both as a player and a coach over the last 30 years, it has been a great journey."
England performance director Mo Bobat added: "Neil has a proven track record of developing world-class pace bowlers and, at a time when we have an abundance of pace-bowling talent, having someone of his quality to oversee their progress, as well as work with counties on their programmes, represents a real asset for us.
"In addition to supporting the six players currently on pace bowling development contracts, Neil's coaching will focus primarily at Lions level, but will also see him move up and down the pathway, working with England bowlers and our Young Lions programme."