Swastikas were discovered painted on two synagogues in the ultra-Orthodox city of Bnei Brak on Saturday morning.
Pictures of Shira Banki, a 16-year-old who was stabbed to death at the 2015 Jerusalem Pride Parade by an ultra-Orthodox attacker, scattered at their entrances.
Prime Minister Naftali Bennett condemned the attacks on the synagogues, calling them "acts of hatred and incitement."
"Desecrating holy sites in Israel, including the disrespectful use of the image of Shira Banki who was murdered, is a wicked act," Bennett said, vowing that the police will bring the perpetrators to justice.
Police are investigating the incident, but have not yet located any suspects.
Both houses of worship serve an ultra-Orthodox and religious Zionist congregation.
A congregant of one of the synagogues said that when worshipers arrived for prayers on Saturday, they were met with the Nazi symbol. "We have Holocaust survivors among us, and this was a very difficult experience for them," he said.
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Another worshiper expressed his dismay on Facebook, writing that "Our synagogue is a place of unity between all denominations."
Rabbi Asher Landau, who runs one of the congregations, said that "In our synagogue, we have Holocaust survivors with numbers etched onto their arms and the children of Holocaust survivors."
He added, "I expect that this awful and disgusting act will be condemned by all of the rabbis and leaders, in a conversation that will contribute to unity rather than divisions."
Foreign Minister Yair Lapid wrote on Twitter Sunday morning that he calls on the police "to quickly investigate and find the person who drew the swastikas in the Bnei Brak synagogues. The person who committed this terrible act must face the full force of the law."
Public Security Minister Omer Bar-Lev, who oversees the police, Tweeted that the daubed swastikas and vandalism "also dared to desecrate the memory of Shira Banki – a girl who was nothing but light, beauty and love of the other." He added that the assailants will be caught, "and they will pay for this. Shame on them."