The rising star of the Israeli right, Naftali Bennett, told the Guardian on Monday, he wants the Jewish state to annex most of the West Bank and that he is against a Palestinian state:

"It's just not going to happen. A Palestinian state would be a disaster for the next 200 years."

If the opinion polls are right, Bennett's party, the pro-settler Jewish Home, will be the second largest in the Israeli Knesset after this month's general election and so likely to be an important player in Prime MinisterBinyamin Netanyahu's next government. If that happens, what is the pro-Israel position for American politicians and activists to take?

Will it be the unquestioning support for the policies of the Israeli government of the day, no matter how misguided the policy advocated by the American Israel Public Affairs Committee (Aipac) and docilely adhered to by members of Congress? Or will it be as Chuck Hagel, the president's nominee for defence secretary, would have it: to continue to assure Israel's military security but to maintain that support for Israel rises above automatic backing for any given Israeli government, which may be pursuing policies that threaten the very existence of the Jewish state.

Anyone who believes that Israel's future is secured by shedding itself of occupation and working to establish a viable Palestinian state cannot doubt that the true friends of Israel are those prepared to act as a sort of loyal opposition in telling its governments, as they move ever further to the right, that they are endangering the future of the Jewish state with the perpetual expansion of settlements, the disparaging of Palestinian leaders committed to a negotiated two-state solution, the attempts to make it all but impossible for East Jerusalem to be the capital of an independent Palestine, and by maintaining the oppression of another people in a way that increasingly eats at Israel's claim to be democratic.

That has been Hagel's position and his nomination raises the prospect that there may finally be a visible debate in the US about what it now means to be pro-Israel.

The defence secretary nominee has been vilified by those who claim to speak for Israel's interests. The language says it all. Critics of policies that might reasonably be regarded as making the Jewish state less secure are accused of "demonising" Israel and harbouring "hatred" for the Jewish state. Increasingly, in recent years, such critics have also been smeared as antisemites. Elliott Abrams, the neocon former special assistant to the president and ex-national security council official,suggested exactly that on national public radio (NPR) when he said Hagel "seems to have some kind of problem with Jews".

Among the particular problems Hagel's critics have is his refusal when a senator to routinely sign Aipac-sponsored letters of unquestioning support for Israeli policies. He would not, for example, put his name to letters pledging unequivocal backing for Israel after the second Palestinian uprising began in 2000, pressing the European Union to declare Hezbollah in Lebanon a terrorist organisation and demanding that the Palestinian leadership bar Hamas from running for election.

Hagel, in an interview with the Lincoln Journal Star in his home state of Nebraska on Monday, said critics have "completely distorted" his record. He said there is "not one shred of evidence that I'm anti-Israeli, not one [Senate] vote that matters that hurt Israel". Which is true.

But his detractors have done that to discredit him because they don't want to talk about what really alarms them: what Hagel did say and his reasoning for it.

"I didn't sign on to certain resolutions and letters because they were counterproductive and didn't solve a problem. How does that further the peace process in the Middle East? What's in Israel's interest is to help Israel and the Palestinians find some peaceful way to live together."

He later added:

"Furthering the peace process in the Middle East is in Israel's interest."

In other words, Aipac is not acting in Israel's best interests but providing political cover in Washington for Netanyahu.

Hagel also got into trouble for pointing out that Aipac "intimidates" members of Congress. Aipac denies this while also claiming to its supporters to be immensely influential in shaping support for Israel on Capitol Hill. But there's no doubt that members of Congress view Aipac much as they view the National Rifle Association – the be crossed only at dire electoral peril.

However, this insistence on unwavering support for Netanyahu (or any other Israeli prime minister) is helping to drive away the very people Aipac claims to speak for. Bradley Burston, an American Jew who settled in Israel, wrote in Haaretz recently that many Jewish Americans are turning away from the state founded in their name:

"In fact, as the new year dawns, there are mounting signs that 2013 may be the year in which US Jews – in the main, liberal in outlook, committed to tolerance, pluralism, and a vigorous, sincere pursuit of peace – effectively secede from this state of Israel. Many American Jews are already distancing themselves in word and deed from a government it sees as arrogant and short-sighted, enslaved to a runaway train of settlement, dismissive of the rights of Palestinians and other non-Jews, cold to the concerns of a sinking middle class and the drowning disadvantaged, contemptuous of the concerns of the larger Jewish world."

Further evidence that Chuck Hagel is right, and that the pro-Israel position is to stand up to Netanyahu.