Ed Miliband's position on Israel has been attacked by former Labour ministers, Jewish party supporters and the Jewish Leadership Council.
The Labour leader has adopted an increasingly tough stance, calling Operation Protective Edge "wrong and unjustifiable" and he has attacked David Cameron for not opposing Israel's actions.
"His silence on the killing of hundreds of innocent Palestinian civilians caused by Israel's military action will be inexplicable to people across Britain and internationally," Mr Miliband said.
Downing Street responded: "We are shocked that Ed Miliband would seek to misrepresent that position and play politics with such a serious issue."
And one former Labour minister said: "Just look at his record. He likes to pretend he's driven by some moral compass but the truth is he's the most cynical leader Labour has ever had. Syria, now Israel. He'll sell anyone out for a vote."
Another senior party figure said he was "ashamed to be in the same party as this excuse for a leader".
Kate Bearman, a former Labour Friends of Israel director, quit the party after 20 years as a supporter as Labour had "chosen to disregard the culpability of Hamas" and was "not fit to govern".
The JLC said: "It is not credible to suggest that the situation can be resolved simply by calling for a ceasefire, when over recent weeks Hamas has brazenly breached six ceasefires and abused them to perpetrate further attacks.
"This is a critical issue and we hope that such an important matter will not be used to create domestic political points of difference."
Many Israel-supporting Labour MPs used the Parliamentary recess to avoid responding to their leader's stance. But on Twitter, Rachel Reeves MP, a Labour Friends of Israel officer, praised Mr Miliband's "important" statement.
Leading Jewish Labour supporters admitted that the situation facing Israel advocates in the party was "grim".
Pointing out that many of the party's strongest Israel supporters were shadow cabinet members, one queried: "Should we tell them to resign over it? Unfortunately, they have to say one thing in private and something different in public. They are whipped. We are only nine months from an election.
"People will not appreciate a possible future prime minister looking like he is point scoring."
Former Labour MP Eric Moonman said Mr Miliband had received poor advice. "The events in Israel are stretching his knowledge," he said.
He said it had been a mistake to attack Mr Cameron, and he could come to regret his comments.
There were further fears that Labour backbenchers and grass-roots activists might use the fall-out from the conflict to consider stronger measures against Israel at their annual conference next month.