WASHINGTON — Justices across the ideological spectrum teamed up during Supreme Court oral arguments on Wednesday to voice skepticism about the N.C.A.A.’s position that it could bar relatively modest payments to student-athletes in the name of amateurism despite the antitrust laws. But some of the same justices also seemed worried about opening the floodgates to further challenges.

Justice Brett M. Kavanaugh said that “the antitrust laws should not be a cover for exploitation of the student-athletes,” adding that he doubted that college sports fans understood amateurism to require it.

“To pay no salaries to the workers who are making the schools billions of dollars on the theory that consumers want the schools to pay their workers nothing,” he said, seems “entirely circular and even somewhat disturbing.”

Justice Clarence Thomas noted that other participants in college sports are paid enormous sums. “It just strikes me as odd that the coaches’ salaries have ballooned,” he said, “and they’re in the amateur ranks, as are the players.”

By contrast, Justice Elena Kagan said, colleges and universities have used their combined market power “to fix athletic salaries at extremely low levels, far lower than what the market would set if it were allowed to operate.”

A ruling in favor of the education-related payments at issue in the case would be among the largest breakthroughs to date in the effort to pay college athletes, which has gained momentum in recent years as one state after another considers proposals to allow them to profit from their fame. It would also be yet another blow to the N.C.A.A., which has found its business model increasingly under siege and has argued that payments would effectively professionalize students.

Though there seemed to be something like a consensus for the payments at issue, several justices said they were concerned that such a ruling would prompt a deluge of other challenges.

“How do we know,” Justice Sonia Sotomayor asked, “that we’re not just destroying the game as it exists?”

Justice Stephen G. Breyer added, “I worry a lot about judges getting into the business of deciding how amateur sports should be run.”

Last year, a federal appeals court ruled that the N.C.A.A. was not free to limit benefits tied to education for Division I football and basketball players. The decision allowed payments for things like musical instruments, scientific equipment, postgraduate scholarships, tutoring, study abroad, academic awards and internships. It did not permit the outright payment of salaries.

The court rejected the N.C.A.A.’s argument that compensating athletes would alienate sports fans who prize students’ amateur status. “Uncapping certain education-related benefits would preserve consumer demand for college athletics just as well as the challenged rules do,” Chief Judge Sidney R. Thomas wrote for a unanimous three-judge panel of the U.S. Court of Appeals for the Ninth Circuit, in San Francisco.

“Such benefits are easily distinguishable from professional salaries,” he wrote, as they are linked to education and could be provided in kind rather than in cash. “The record furnishes ample support,” Judge Thomas added, “that the provision of education-related benefits has not and will not repel college sports fans.”

At the argument on Wednesday, Seth P. Waxman, a lawyer for the N.C.A.A., said “these new allowances are akin to professional salaries.”

Chief Justice John G. Roberts Jr. responded that some of the payments the association already allows had a similar character.

“Schools can pay up to $50,000 for a $10 million insurance policy to protect student-athletes for future earnings,” he said. “Now that sounds very much like pay for play.”

Justice Samuel A. Alito Jr., drawing on briefs supporting the players, painted a bleak picture of athletes’ lives and futures.

“They face training requirements that leave little time or energy for study, constant pressure to put sports above study, pressure to drop out of hard majors and hard classes, really shockingly low graduation rates,” he said. “Only a tiny percentage ever go on to make any money in professional sports.”

“So the argument is they are recruited, they’re used up, and then they’re cast aside without even a college degree,” he said. “How can this be defended in the name of amateurism?”

Mr. Waxman said the alternative would be worse. “If you allow them to be paid,” he said, “they will be spending even more time on their athletics and devoting even less attention to academics.”

Justice Alito said the athletes were already paid. “They get lower admission standards,” he said. “They get tuition, room and board, and other things. That’s a form of pay. So the distinction is not whether they’re going to be paid. It’s the form in which they’re going to be paid and how much they’re going to be paid.”

Mr. Waxman said paid internships posed particular hazards because they could involve unlimited sums.

Justice Sotomayor responded that the N.C.A.A. remained free to set limits. “If you think that internships should be related in some way to the educational experience,” she said, “you could pass rules to that effect.”

Justice Thomas said that paying athletes “sounds fine for the upper-level schools, whether it’s, you know, Alabama, Ohio State and Nebraska.” But he said he was worried that “the bigger schools would begin to cherry-pick with the transfer portal the athletes from the lower schools simply because they’re able to afford this income.”

Jeffrey L. Kessler, a lawyer for Shawne Alston, a former West Virginia University running back, and other student-athletes challenging the N.C.A.A.’s rules, said that “those schools don’t compete now.”

“Alabama pays its weight coaches $700,000 a year,” he said. “None of those small schools can do that.”

The Supreme Court last considered how antitrust laws applied to the association in 1984, ruling that its restrictions on television coverage of college football games were unlawful. But the decision, National Collegiate Athletic Association v. Board of Regents of the University of Oklahoma, included an influential passage on student-athletes.

“The N.C.A.A. plays a critical role in the maintenance of a revered tradition of amateurism in college sports,” Justice John Paul Stevens wrote for the majority. “There can be no question but that it needs ample latitude to play that role, or that the preservation of the student-athlete in higher education adds richness and diversity to intercollegiate athletics and is entirely consistent with the goals of” the antitrust laws.

The Biden administration filed a brief supporting the athletes in the new case, National Collegiate Athletic Association v. Alston, No. 20-512, saying that the Ninth Circuit had struck the right balance.

“The court was focused on legitimate educational expenses,” Elizabeth B. Prelogar, the acting solicitor general, told the justices on Wednesday.

Besides the coronavirus pandemic, no issue has recently demanded more of the N.C.A.A.’s attention than the rights of student-athletes, especially whether they should be able to profit from their fame. College sports executives have long feared that loosening age-old rules would open a different array of challenges, but they have faced mounting pressure over the past few years from Congress and many of the nation’s statehouses.

Most crucially, a Florida law that directly challenges the N.C.A.A.’s policies is scheduled to take effect this summer, and California legislators are considering a proposal to speed up a similar measure there.

Although the N.C.A.A. has vowed to rewrite its rules, it delayed final approval over the winter after the Trump administration’s Justice Department raised misgivings. And Congress has not rushed to give the association the kind of political and legal cover it craves.

The argument on Wednesday had some lighter moments, as when Mr. Waxman mistakenly addressed Justice Thomas as “Mr. Chief Justice.”

“Thank you for the promotion,” Justice Thomas said.

The chief justice responded that the job was taken. “There’s no opening, Mr. Waxman,” he said.