The 54-year-old Jol joined Ajax in 2009 from German club SV Hamburg and they finished second in the league in his first season, won the Dutch Cup and qualified for the Champions League group stage.
Jol, linked with the new vacancy at English Premier League Newcastle United, started his coaching career with Dutch clubs Roda JC Kerkrade and RKC Waalwijk before joining England's Tottenham Hotspur as manager.
"With pain in my heart I will leave this beautiful club," Jol said.
"Last year summer we started something which I would like to have finished but I realised that the expectations after last season were to high.
"We could not fulfil those expectations and that hurts. The number of critics the club has to deal with on a daily bases causes unrest in the organisation and the squad."
Former Dutch international Frank de Boer, an assistant to Netherlands coach Bert Van Marwijk, will take charge of Ajax on a provisional basis until the winter break starting on December 24.
Ajax play away at AC Milan in the Champions League on Wednesday and need a win to secure a place in the Europa League.
They lie fourth in the Dutch League midway the season, five points behind leaders PSV Eindhoven and Twente Enschede.
Newcastle fired Chris Hughton as their manager on Monday. Hughton worked as Jol's assistant at Tottenham.
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