Brigadier General Dan Goldfus, head of the 98th division deployed in Gaza's main southern city of Khan Yunis, also appeared to enter into a row over exempting ultra-Orthodox Jews from military service.
He was subsequently summoned by the military leadership for his comments, which breached a long-standing taboo on uniformed officers publicly wading into politics.
"You must be worthy of us," Goldfus said of his country's leaders, in comments broadcast on Israeli television on Wednesday.
He called for Israeli politicians "to push aside the extreme, and adopt togetherness" in the Gaza war sparked by Hamas's October 7 attack on southern Israel.
The general vowed that military commanders and soldiers would take responsibility for their actions.
Prime Minister Benjamin Netanyahu has so far stopped short of assuming personal responsibility for Israel's intelligence failures on October 7 and said any official investigations must take place after the war.
"We will not run from responsibility. We bow our heads in light of our reverberating failure on October 7, but at the same time are leading forward," the general said.
Since Israel launched a ground offensive in Gaza on October 27, 249 soldiers have been killed in the Palestinian territory, according to the military.
Addressing Israel's political leaders, Goldfus called on them to ensure that "everyone takes part" in enlisting in the armed forces, in an apparent reference to ultra-Orthodox Israeli men being exempt from national service -- a contentious political issue.
Most Jewish men are required by law to serve in the Israeli military, but members of the ultra-Orthodox minority -- known in Hebrew as Haredim -- have long been given sweeping exemptions.
Since the October 7 attack by Hamas, public frustration over the exemption has resurfaced, adding pressure on Netanyahu's governing coalition, which relies on ultra-Orthodox allies staunchly opposed to drafting Haredi men.
Neither Netanyahu nor Defence Minister Yoav Gallant publicly responded to Goldfus's remarks.
Some lawmakers voiced their approval while others expressed dissatisfaction with the general making political statements of any kind.
Yoav Segalovitz, a centrist opposition lawmaker, told Kan public radio on Thursday that "a uniformed officer needs to talk only about what's related to his decisions or take off the uniform".
Writing in the Yedioth Ahronoth newspaper, columnist Nahum Barnea said that "with all respect to the heartfelt sentiments of the esteemed officer, fighting in Gaza doesn't give him the right or the authority to express a position on political matters".
Hamas's October 7 attack resulted in the deaths of about 1,160 people in Israel, mostly civilians, according to an AFP tally of official Israeli figures.
Israel's subsequent retaliatory offensive in Gaza, aimed at destroying Hamas, has killed at least 31,341 Palestinians, mostly women and children, according to the health ministry in the Hamas-run territory.
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