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"I can no longer reconcile my commitment to the role and to the financial services sector with the complete lack of confidence in your continuing leadership of our country," Glen said in his letter to the prime minister.
His resignation comes after finance minister Rishi Sunak and health secretary Sajid Javid both announced their departures abruptly late on Tuesday.
Britain's financial sector, one of its most important tax-raising industries, was largely cut off from the European Union after Brexit, with banks and insurers now piling pressure on the government to buttress the City of London's global competitiveness.
Glen, who often joked he was Britain's longest serving City minister, was first appointed in January 2018.
He has undertaken over 30 public consultations and reviews on post-Brexit financial reforms.
The sector has long urged the government to speed up the pace of reform, whose timing is now thrown into doubt by political uncertainty.
Sunak was due on July 19 in a speech at the Mansion House in the City to set out a new financial services law to ease rules on insurers, capital markets and encourage more retail investing by exploiting Britain's post-Brexit "freedoms" to write its own regulations.