David Cameron has resisted party pressure to adopt a more hardline response to Israel's actions in Gaza.
Backbench efforts to force a change in position were boosted when Foreign Office minister Baroness Warsi quit because she could no longer support the government line.
In her resignation letter, she wrote: "Our approach and language during the current crisis in Gaza is morally indefensible."
Her decision gave rise to concerns that another minister may resign, and former attorney-general Dominic Grieve questioned whether Israel's actions were "necessary and proportionate".
A Downing Street spokesman said Mr Cameron regretted the resignation but reiterated the fact that the government had repeatedly called for a ceasefire, although he had repeatedly refused to condemn Israel's actions in stronger terms.
Leading Jewish party supporters tried to downplay the reaction, citing internal party wrangling as a key motivation for those attacking Israel.
One Westminster source said: "Warsi was a nonentity. Cameron kept her around for electoral reasons. She knew she would be on her way soon.
"The feeling is that most people will support the government line. In terms of cabinet members, things are good. A lot have just got promoted and won't give that up."
Media reports on Wednesday suggested Mr Cameron had been "stunned" by senior colleagues' "revolt" on the issue, but Israel supporters in the party said the matter had been "totally over-egged".
"There are a handful of dissenters," said one. "Boris Johnson went a bit off the reservation but that might just be Boris being Boris."
The London Mayor, normally a strong supporter of Israel, had said its military action was "disproportionate and tragic".
That led the London Jewish Forum to seek a meeting with him. Its chairman, Adrian Cohen, said: "The last thing London needs is for the mayor to add fuel to the flames by bringing the Middle East into London politics."
Stourbridge MP Margot James, who previously joined a Conservative Friends of Israel delegation to the country, wrote to Foreign Secretary Philip Hammond to express dismay at the "unjustifiable" scale of Palestinian suffering.
Sir Nicholas Soames, Mid-Sussex MP, said Israel's actions "are beyond the pale" and the government's response was feeble.
MP for Totnes, Sarah Wollaston tweeted on Monday: "On a day we pause to remember the fallen of WW1, Israel resumes the mass slaughter of innocents".
In his strongest comments on the crisis, Mr Hammond accepted last weekend that the public was "deeply disturbed" by the suffering and that the situation had become "intolerable".
He said he was concerned that antisemitism would continue to rise in Britain.