Lila Tretikov wrote in an email that it was time for her to move on.
A leaked memo suggesting the Foundation was looking at creating a "commerce-free" search engine had upset the volunteer Wikimedia community.
Many were angry that it had not been discussed first, as transparency is key to the ethos of the organisation.
In September 2015, Wikimedia was awarded a $250,000 grant from a trust called the Knight Foundation for work to "advance new models for finding information by supporting stage one development of the Knowledge Engine by Wikipedia, a system for discovering reliable and trustworthy public information on the internet," according to a document uploaded by Wikimedia itself.
The project summary at the end of the document - although its author is unclear - states that the Knowledge Engine would be "the world's first transparent search engine, and the first one originated by the Wikimedia Foundation".
The leaders of the team were listed as Ms Tretikov, vice-president Wes Moran and Wikimedia head director of search and discovery Tomasz Finc.
However, in published notes from a meeting to discuss the controversy, Ms Tretikov is recorded as saying the grant news had been shared "without context".
A new team had been set up, given the task of researching "how Wikimedia users seek, find, and engage with content", Ms Tretikov wrote in a piece co-authored with Mr Moran.
But they went on to deny that a search engine was the intended outcome.
"What are we not doing? We're not building a global crawler search engine," they wrote.
"We're not building another, separate Wikimedia project... Despite headlines, we are not trying to compete with other platforms, including Google."
Wikipedia editor William Beutler recently told the website Motherboard that the controversy was the result of a "culture clash" between the Foundation and its volunteers.
"The community is this volunteer group that is made up of people who largely buy into Wikipedia for ideological reasons," he said.
"Then you have the Foundation, which has increasingly fewer people from the community and a larger Silicon Valley contingent that comes from a tech background."
The Wikimedia Foundation has been contacted by the BBC for comment.

Bruno Travalja, 52, was kneeling to take a measurement on the 42nd floor of the Manhattan building when he stood up and felt "dizzy", say police reports.
His body was found between 52nd and 53rd streets in midtown on Thursday afternoon, according to local media.
Officials are investigating whether faulty equipment or any violated safety protocols were factors in the death.
It is thought the New Jersey architect fell from the former Flatotel, which construction crews are converting into condominiums and offices.
The NYPD and the city's Department of Buildings are investigating the incident.
Mr Travalja was the owner of Crown Architectural Systems, according to his Facebook page.
Cetra/Ruddy, the architectural firm of record on the project, did not immediately respond to a request for comment.
The executive director of the Wikimedia Foundation, which runs Wikipedia, has resigned after denying the group is considering building a search engine.
[NEXT_CONCEPT]
An architect has fallen to his death from a New York City skyscraper after losing his footing while at work.