"Interpreting 'sex' to mean gender identity would generate conflicts with religious persons and institutions across a range of fronts," wrote the groups, which include organizations within the Islamic, Jewish and Christian traditions.
The opposition marks the latest in the LDS Church's evolving approach to transgender rights as Americans debate appropriate levels of protection for lesbian, gay, bisexual and transgender individuals.
After the Obama administration directive came out last year, Mormon leaders didn't directly oppose or support the move, but rather called on public officials to create rules that balance safety, privacy and dignity for all while urging "people of goodwill" to find "reasonable solutions."
In 2015, LDS leaders gave their blessing to a state law that protects the LGBT community against housing and workplace discrimination while safeguarding some religious freedoms.
"This movement arose after centuries of ridicule, persecution and even violence against homosexuals," Neill F. Marriott, second counselor in the faith's Young Women General Presidency, said at the time. "Ultimately, most of society recognized that such treatment was simply wrong."
Just last month, the LDS Church didn't take a stand for or against the Boy Scouts of America's decision to allow transgender children to join its boys-only programs, saying it is studying the issue.
"Boy Scouts has assured its religious chartering organizations that, as in the past, they will be able to organize their troops in a way fully consistent with their religious beliefs," the faith said in a news release.
The latest court brief goes beyond these sentiments, but LDS leaders insist the filing doesn't mark a change in church policy. Instead, it expresses a desire for the justices to let Congress and statehouses develop policies on the transgender issue.
"The brief concludes by arguing that, instead of imposing an outcome Congress did not intend, the Supreme Court should allow Congress and state legislatures to reach compromises where transgender persons can be appropriately accommodated without infringing on the free exercise of religion, while seeking fairness for all," church spokesman Eric Hawkins wrote in an email. "Sustainable results will be more likely achieved if citizens and lawmakers are left free to address gender identity in ways that preserve the nation's priceless heritage of religious freedom."
Neca Allgood, a Mormon mother of a transgender son, said the church's policy is far from clear.
"My own experience is that the church has very little in the way of a policy forthrightly stated about transgender people," the Syracuse resident said, noting that the faith doesn't change its rolls if a member identifies with a gender different than the one at birth.
"I was not at all clear on why the church would choose to take a position on that interpretation of Title IX," Allgood said of the decision to file a brief. "It doesn't seem like a religious liberty question to me."
The transgender question, however, may be a doctrinal issue within Mormonism. The faith's oft-referenced 1995 proclamation on the family says "gender is an essential characteristic of individual premortal, mortal and eternal identity and purpose."
Lynn Wardle, a law professor at LDS Church-owned Brigham Young University, said Mormon leaders rarely get involved in such legal cases and that the religious groups' statement sends a message to the court.
"Generally, the church institutionally avoids taking positions on specific legislative proposals," Wardle said, acknowledging its public efforts against same-sex marriage. "When they feel that a core interest of the church as an institution or as a community of believers is imperiled, they have taken positions."
The American Civil Liberties Union said other religious organizations, which support the Department of Education directive, will weigh in with the court.
"We expect to hear from other religious leaders," the ACLU wrote in a statement, "who will explain why it's important to their faith and values that transgender people are treated with the same dignity and respect as everyone else."