Some are demanding the mostly Iranian-backed forces be disbanded but the militias say their sacrifices on the battlefield and the fact they were sanctioned by Iraqi Prime Minister Haider al-Abadi have earned them a permanent place in the hierarchy of Iraq's security forces.
The Shiite militias stepped into a vacuum when the Iraqi army largely dissolved after IS overran Mosul and pushed within 80 miles (130 kilometres) of the Iraqi capital.
Tens of thousands of men, many of them members of the long-established Shiite militias with close ties to Iran, answered al-Sistani. In the days that followed, Iraq was flooded with training, money and weapons from Tehran.
Billboards praising the groups, depicting Iraqi and Iranian paramilitary leaders side by side, popped up across Baghdad, alongside posters of martyrs honouring the fallen.
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Although the Shiite militias did not play a central role in the battle for the city of Mosul itself, they moved into the deserts held by IS west of the city, massing around the town of Tal Afar and taking a border crossing between Iraq and Syria. They also took control of highways bisecting the Sunni heartland in western Iraq and used as vital military and civilian supply lines.
In past fights against IS, including the operation to retake for the cities of Tikrit and Fallujah, the Shiite militias were accused of sectarian killings and other abuses against minority Sunnis. They acknowledge some abuses may have occurred but say those responsible have been disciplined.
"We always knew that Iran would use this (call to arms) to increase its own power in Iraq, but we had no other choice," said al-Bidayri, recounting the meeting in Najaf and the panic-filled days after the 2014 fall of Mosul.
Al-Bidayri says now that Mosul has been retaken and the Iraqi military has been partially rebuilt, he believes the Shiite militias should be disbanded, to curb Iranian influence in Iraq and reduce sectarian tensions. The elderly sheikh, like much of Iraq's religious establishment in Najaf, is a staunch nationalist and wary of Iran's growing influence.