The 68-year-old, who won eight Eredivisie titles and three European Cups with the Dutch giants, has stepped down from the position after growing disillusioned with his impact.
It has been five years since Cruyff's 'velvet revolution' took place in the Amsterdam Arena, with a view to making youth production a top priority for the club. Meanwhile, former Ajax players Marc Overmars and Edwin van der Sar were put into administrative roles, taking over as technical director and marketing director respectively.
The club has been caught in a public feud in recent days surrounding their attempt to fire Wim Jonk - the head of youth development and last faithful follower of the Cruyff plan.
Jonk has refused to leave his post, while his fellow coaches in the youth system have publicly voiced their support of him, but the turmoil is too much for Cruyff, who will no longer advise the club.
"I quit," he wrote in his column in De Telegraaf. "For years I have noticed that the core of my vision within Ajax hasn't been followed up.
"In addition, I increasingly got the feeling that this has been done deliberately, and I do not play games.
"Of course this feels like a raw deal. I'm just a director and I had high hopes that the whole thing would be in good hands with a few experienced drivers.
"Those in charge at Ajax must sit together and look first at themselves. Make sure it will be fine, but it will not happen under the umbrella of the Cruyff-plan, because my name will not be there anymore."