Appointed in July 2013 after switching from Croydon, the duo guided Leafe into the Ryman League as Southern Counties East League champions before reaching the Ryman South play-offs the following season.
The pair decided to call time on their stay at Church Road after last Saturday's 5-2 defeat at Ramsgate, a sixth league reverse of the season that left their side sitting 19th in the table.
In a statement on Wednesday naming Rob Smith and Danny Rose as joint caretakers while the hunt starts to replace them, Leafe officials paid tribute to their outgoing management team.
A spokesman said: "The club would like to express its gratitude to John and Dean for their loyalty and commitment to the club over the last four seasons."
After guiding the club to a 5-4 win over Westfield in the first round of the Surrey Cup on Tuesday night, Smith and Rose are expected to be at the helm on Saturday when Leafe host Ryman North Cheshunt in the preliminary round of the FA Trophy.
Potential candidates for the vacant manager's post should send their footballing CVs to Whyteleafe chairman Mark Coote at: chairman@whyteleafesoccer.co.uk.
Image courtesy of www.theleafe.co.uk
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