For the first time since 1983, the United States Supreme Court is taking on a case that could overturn its long-held approach to deciding when government-endorsed prayer in the public square violates the Constitution.

The case, which involves an upstate New York town whose legislative meetings opened with prayer invocations that were given almost exclusively by Christian ministers, has many Jewish groups preparing to weigh in with briefs calling for maintenance of a strong separation between religion and state.

But one prominent Jewish attorney with widely recognized expertise on church-state law has already filed a brief meant to dissent from that communal consensus.

“It’s important to show the court there is no unanimous Jewish view against prayer,” said Nathan Lewin, a veteran Washington attorney whose clients have included everyone from the late John Lennon to former attorney general Edwin Meese. “I don’t think we benefit from being seen as those who wish to eradicate religion from the United States.”

For Lewin, the case of Town of Greece v. Susan Galloway and Linda Stephens is yet another opportunity to express the Jewish community’s minority voice, opposing restrictions on public practice of religion.

The case, which will be heard in the fall, takes on the question of opening legislative sessions in Greece, N.Y., that were delivered, in all but a handful of cases, by Christian clergy. The Supreme Court’s decision to accept the case that directly challenges the established legal status quo on public prayer could reflect shifting positions within the highest court since it last faced the issue, three decades ago.

The Town of Greece is located in New York State’s Monroe County, just outside Rochester, and is home to 96,000 residents who are predominantly white and Christian. Since 1999, the town had opened all its legislative meetings with a prayer delivered, almost always, by Christian clergymen.

In 2008, following complaints by two locals regarding the exclusively Christian nature of the prayers, the town invited a Jewish lay leader, a Wiccan priestess and the chairman of a local Baha’i congregation to deliver the opening invocation. But the local complainants remained uncomfortable with the overall Christian content of the prayers. Their decision to take the case to federal court led to a ruling that put an end to the prayers altogether on the grounds that they violated the Constitution’s Establishment Clause.

In reviewing the case, the Second Circuit Court of Appeals affirmed the lower court, ruling that the town’s prayer practices “must be viewed as an endorsement of a particular religious viewpoint.” The court cited the town council’s selection process, which led to an almost exclusively Christian list of prayer givers and to the religious content of the prayers themselves. The Supreme Court agreed to take on the appeal in May. Arguments will be heard in the fall, and a decision is expected by next summer.

More than two dozen groups and individuals have filed friends-of-court briefs supporting the Town of Greece. They include the federal Department of Justice, which argued for upholding the practice of legislative prayer; members of Congress; 23 state attorneys general, and a group of theologians. Standing out in the list of supporters is Lewin, the lone Jewish voice in support of continuing the town’s Christian prayer.

The brief filed by Lewin reads as much like a talmudic discussion as it does a legal argument. Lewin draws on recent-day sages Rabbi Moshe Feinstein and the late Lubavitcher rebbe Menachem Mendel Schneerson to make the case that Jewish religion and tradition are not opposed to Christian prayer. “Authentic Jewish attitude toward Christian prayer,” Lewin wrote, “is encouragement, not condemnation.” Lewin also quotes from the books of Genesis, Kings I, Jonah and Isaiah in making the case that Jewish scripture does not include any opposition to non-Jewish prayer.

Another argument presented in Lewin’s brief is that the United States Congress itself has long opened its legislative sessions with a religious prayer and that rabbis have been invited numerous times to deliver the prayer. The first such invitation, he noted, was in 1860, to Rabbi Morris Raphall, who appeared before Congress “piously bedecked in a white tallit and a large velvet skullcap.”

Lewin is well aware of the fact that he is breaking ranks with the organized Jewish community. In fact, that is one of the reasons he filed his brief. “I’m going against the reflexive unthinking mainstream,” he said, referring to major Jewish organizations. “People say. ‘Oh, God, there’s a prayer that says something Christian, so we should oppose it.’”

Lewin, who is 76 and shares a Washington practice with his daughter Alyza, has been at the forefront of church and state battles for decades, always representing a school of thought closer to that of the Orthodox minority in the Jewish community — one that, in general, is more willing to challenge the definition of church and state separation.

A former clerk for Supreme Court justice John Harlan, and a lawyer in Robert F. Kennedy’s Department of Justice, Lewin, whose father was a senior figure in the ultra-Orthodox group Agudath Israel of America, has long taken on legal issues relating to Jews and to the Orthodox Jewish community in particular. In 1989 he successfully argued the case of County of Allegheny v. American Civil Liberties Union, in which Chabad of Pittsburgh won the right to keep its 18-foot Hanukkah menorah outside the city-county building. (In the same case, the Supreme Court ruled against presentation of the nativity scene in the county courthouse.)

Lewin also represented Sholom Rubashkin, the former head of Agriprocessors kosher meat plant. Rubashkin was sentenced to 27 years in prison for fraud and money laundering. Lewin called the court decision “the greatest injustice” he has seen in 50 years of practicing law.

More recently, Lewin suffered a loss when the court rejected his attempts to force the Obama administration to register Israel as the birthplace of Americans born in Jerusalem.

As Lewin and other supporters of legislative prayer prepare their court filings in advance of the Town of Greece hearing, opponents, many of them from the organized Jewish community, are rallying their forces against them.

The Anti-Defamation League intends to join the case in support of upholding the lower court’s restriction on the town’s prayer practices, and other Jewish organizations and religious denominations are expected to add their voices, as well.

“The town is aligning itself with a certain faith, and that sends an exclusionary message,” said David Barkey, ADL’s national religious freedom counsel. He rejected as irrelevant Lewin’s argument that Judaism does not oppose Christian prayer. “The court doesn’t need to make decisions based on what the Jewish faith believes or does not believe,” Barkey said.

For activists involved in the debate, there is much more at stake than the future of an opening prayer at a small town’s legislative meetings.

A Supreme Court ruling overturning the circuit court’s decision could potentially include a call by the highest court to change the tests for determining when a religious expression violates the Establishment Clause. Currently, these tests include examining whether the government actions have a secular purpose, do not advance or inhibit religion, and do not result in excessive government entanglement in religion. Changing the test could mean that only coercive prayer or proselytizing constitutes a violation.

“I’m not very optimistic,” Barkey said.

Much has changed since these tests were put in place, both in America and in the Supreme Court. None of the justices who decided the 1983 Marsh v. Chambers case, which was the last time the court took on state and church issues, is still on the bench. The court refused back then to overturn the tests that have served as the bedrock of determining violations of the Establishment Clause. But that approach may no longer reflect the Supreme Court justices’ views.

Changes are taking place on the state level, where dozens of court cases have been decided in favor of expanding legislative prayer and of funding religious schools with taxpayer dollars.

Lewin says the shift is also felt within the Jewish community, though at a slower pace. The growth of the Orthodox community and its difficulty in funding religious education have increased the voices favoring the lowering of the wall of separation. Lewin noted that when last faced with a church and state issue in Marsh v. Chambers 30 years ago, the Supreme Court heard only from Jewish activists who opposed legislative prayer.

“The Supreme Court must be informed this time,” Lewin said, “that America’s Jewish population is not unanimous in objecting to Christian prayer or in seeking the suppression of pleas for divine blessings at governmental sessions.”

Contact Nathan Guttman at guttman@forward.com or on Twitter, @nathanguttman