Qari Hekmat was the top commander of IS's Afghan franchise in the northern province of Jowzjan, where the group established a stronghold after coming under intense pressure in the eastern province of Nangarhar.
Hekmat was killed Friday in an Afghan airstrike in Darzab district, the defence ministry said in a statement, describing him as "one of the key figures" for IS in northern Afghanistan.
He was involved in or responsible for "deadly terrorist attacks" and has been replaced by Mawlawi Habib-ul-Rahman, the ministry added.
Provincial governor Lutfullah Azizi confirmed Hekmat had been killed but said US Forces carried out the airstrike.
US Forces did not immediately respond to AFP's request for comment.
"Our intelligence sources have identified his body. His death will affect the recruitment of Daesh and disperse IS fighters in Afghanistan's north," Azizi said, using the Arabic acronym for IS.
Afghan and US forces have ramped up airstrikes and ground offensives against IS fighters in Jowzjan in recent months as the group seeks to expand its foothold in the country.
Afghan security forces last month detained a French woman fighting for IS in the same district of Jowzjan. AFP has reported that French and Algerian fighters, some arriving from Syria, have joined IS in the restive province.
In January, Afghan forces caught the group's "head facilitator of foreign forces". Two months later, his two successors were killed in a US airstrike, NATO's Resolute Support mission said previously.
Jowzjan provincial police chief Faqir Mohammad Jawzjani said Hekmat's death was "a big blow" to IS in the north.
"He was the founder of Daesh in northern Afghanistan and had recruited fighters," Jawzjani said. He said Hekmat was killed on Thursday in a joint operation between Afghan and foreign forces.
IS first emerged in Afghanistan in 2014 as NATO combat troops withdrew from the country and handed over responsibility to Afghan security forces.
Despite being vastly outnumbered by the Taliban, IS has claimed responsibility for devastating attacks in Kabul and elsewhere in the country.
Some Western and Afghan officials believe it has received help from the Haqqani Network, a brutal wing of the Taliban.
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