Marko Bandelli quit after apologising for sending an email to an independent candidate in a mayoral election in Komen, in which he indicated that the western city might get no EU funds if the candidate won.
Prime Minister Marjan Sarec had asked Bandelli - himself a former mayor of Komen - to quit on Monday after learning about the email.
Bandelli is a member of the Party of Alenka Bratusek (SAB), a former prime minister, who expressed disappointment that Sarec did not discuss the situation with her before asking Bandelli to resign.
"If the coalition will continue to use such communication channels, our (coalition) time will be short," she said.
In a letter to the prime minister, Bandelli said he made a mistake with the email, which was a result of a dispute between residents in Komen, where Bandelli still lives.
Under the terms of the coalition agreement, SAB will nominate his replacement, which is expected to happen in the coming weeks.
The centre-left government, formed after an election in June, consists of the List of Marjan Sarec, SAB and three other parties. It holds 43 out of 90 seats in parliament and relies on the support of the Left party - which is outside the coalition - to pass legislation.
Tanja Staric, a political analyst at Radio Slovenia, said first indications were that the government had dealt with the issue fairly well.
"As long as there is economic growth and enough money to fuel parties' demands, the government is likely to stay in power, but any significant crisis regarding economy or migration could topple it," she added.
Export-oriented Slovenia, which narrowly avoided an international bailout for its banks in 2013, returned to growth a year later.
The government - which has pledged to raise the minimum wage, public sector wages and pensions as well as defence spending - expects the economy to expand by 4.4 percent this year and by 3.7 percent in 2019.
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