Sweden Democrats (SD) leader Jimmie Akesson called for some mosques to be seized and levelled during a speech to his annual party conference on Saturday.
"We need to start confiscating and tearing down mosques where anti-democratic, anti-Swedish, homophobic, anti-Semitic propaganda or general disinformation is being spread," Akesson said.
Kristersson, whose coalition government does not include SD but relies on its support, condemned the statements as "disrespectful".
"I think it is a disrespectful way of expressing oneself, a polarising way of expressing oneself," Kristersson told broadcaster SVT.
"This misrepresents what Sweden stands for internationally," he added.
Akesson's speech sparked anger both in Sweden and abroad and forced Kristersson to issue a statement on X, formerly Twitter, reiterating Sweden's "constitutional right to freedom of religion".
"In Sweden, we do not demolish places of worship. As a society, we must fight back against violent extremism whatever its grounds -- but we will do so within the framework of a democratic state and the rule of law," he said.
Former Social Democrat prime minister Magdalena Andersson called for Kristersson to remove all SD officials working at the cabinet offices in Stockholm.
"It worsens the image of Sweden, does not facilitate our NATO application and further increases polarisation in our country. This is not putting Sweden and the Swedish people's safety and security first," Andersson said on X.
Sweden, whose NATO application still needs ratification from Hungary and Muslim-majority Turkey, has seen a slew of incidents spark tensions with countries around the Middle East.
A series of Koran-burnings earlier this year led to protests and widespread condemnations of Sweden, with several Middle Eastern countries summoning Swedish envoys.
Iraqi protesters stormed the Swedish embassy in Baghdad twice in July, starting fires within the compound during the second incident.
Last year Sweden was the target of a vast disinformation campaign claiming its social services were "kidnapping Muslim children" and placing them in Christian homes, forcing the authorities to publicly deny the allegations.
