In a Facebook post last week, Listhaug wrote that Labour "thinks the rights of terrorists is more important than the nation's security".
The statement was posted as a graphic using an image of militants wearing face-covering black scarves.
Listhaug used the post to criticise a decision by Labour, led by Jonas Gahr Støre, to vote against a proposal enabling the Ministry of Justice to revoke the citizenship and passports of Norwegians accused of fighting for terrorist groups without any conviction being made against them.
"We want to revoke the passports and citizenship of foreign fighters and terrorists quickly and effectively! Labour wants to vote against. We cannot sit on our hands in the fight against terror!" the minister wrote in the post containing the graphic.
Støre reacted by condemning Listhaug's message.
"The post was made the same day as the Utøya [2011 terrorist attacks committed by Anders Breivik, killing 69 members of Labour's youth party, ed.] film was released at Norwegian cinemas. We have been victims of terror, and we are fighting against terror. For Listhaug to make such a claim so offensive and unfair is disappointing and unbefitting of a Norwegian justice minister," the Labour leader told NRK.
Prime Minister Erna Solberg, after initially declining to comment, later criticised the post.
"I think that occasionally rhetoric overshadows content in politics, and that's what I think happened in this case," Solberg told NRK on Sunday.
"The use of the image, tone and attack on the Labour Party has taken focus off what is an important debate on how to fight terror," the PM said.
But Solberg avoided saying she would ask Listhaug to remove the post.
Progress Party leader Siv Jensen, who is also finance minister, declined to comment on the controversial social media message.
"Last weekend's debate will not affect the government's budget negotiations over the next three days. It is important that we discuss methods in the immigration and integration debate and I agree we should continue to do that," Jensen said at a government budget conference, NRK reports.
A local Progress Party politician said that although he supported the sentiments expressed by Listhaug, he would have done things "differently".
"I would have done it differently and used different rhetoric. I have a different style, but we agree about the content," Progress Party spokesperson in Ulstein Knut Erik Engh told NRK.
"What she means is we must make sure it is not easy for foreign fighters to travel and that there must be a consequence. She thinks Labour has been too weak in its position on this, and they have," Engh said.
Listhaug came in for harsh criticism from Norwegian Facebook users responding to the post, which has over 11,000 reactions and 3,000 shares at the time of writing.
In a comment liked over 1,700 times, Petter Farstad wrote that Listhaug was the "biggest crybaby in parliament".
"As soon as she doesn't get her own way she runs off to her xenophobic supporters to win sympathy. How about a bit of respect for the parliamentary majority? Taking someone's citizenship is something only a court can do and not Listhaug, who is running the errands of racists," Farstad wrote.
"Your job is to uphold Norwegian law. You are not doing that by ignoring it," wrote another user.
Some posts also expressed support for the minister's statement, though these appear to be fewer in number.
Listhaug has so far not responded to NRK's requests for further comment on the issue.