Richmond, Virginia (CNN) Fifteen appellate judges in Richmond on Thursday spent three hours showing how deeply divided they are on whether they can curtail the President's business interests .

In some of the bluntest public arguments yet in court about President Donald Trump's hotel empire, the 4th US Circuit Court of Appeals debated a major case challenging whether Trump can continue to accept emoluments , or profits, from his hotel in Washington while in office.

At times, judges took over from the arguing attorneys, the Justice Department, Trump's personal legal team and the DC and Maryland state attorneys general offices to argue for or against the President themselves.

"We are winging it. If this isn't off the rails, then I don't know what is," said Judge Harvie Wilkinson III, a Reagan appointee who's been on the federal appellate bench at least a half decade longer than any other judge in the wood-paneled room Thursday.

"There are, there are other suits involving congressional subpoenas and everything that presents closer questions, but this one's a lemon," he added. "It's the weakest of the cases that are springing up like jimsonweed against the presidency in this environment."

At this stage, a decision could control whether the case has months ahead of it still in court -- keeping the President's companies at risk as his opponents seek financial documents -- or whether it will be dismissed, a win for Trump. Either way, the issue is likely to eventually reach the Supreme Court.

"We're treating this as if it's some ordinary run-of-the-mill case. It is not," Wilkinson said. He quickly became one of the President's staunchest defenders in court Thursday outside of Trump's own attorney and the Justice Department.

Several other judges, appointed by Democrats, expressed their doubt nearly as sharply with the Justice Department's arguments and Trump himself.

"Nothing can be done?" Judge James Wynn Jr. asked, citing rooms being sold at Trump's Mar-a-Lago resort in Florida to foreign governments and the larger question of whether the President is above the rule of law. What can the judiciary do when the President "openly and without any reservation violates the law?" Wynn pressed a Justice Department attorney in court. "No president has done this."

Wilkinson countered him, pointing out that Congress and politics generally can curtail the president's behavior. The judge mentioned the recent announcement and withdrawal of a plan to hold the G7 convention at Trump's Doral resort in Florida following "immense pressure."

and to their residents, according to the lawsuit. The two governments had The case is one of three currently before federal appeals courts testing Trump's business interests and the emoluments clause. In this case, Maryland and DC governments say they have been harmed because foreign governments and officials from US states choose to stay or hold events at the Trump International Hotel in Washington to ingratiate themselves with the President. This is unfair to businesses owned by DC and Marylandand to their residents, according to the lawsuit. The two governments had subpoenaed the Trump Organization and federal agencies before that evidence collection was put on hold by the appellate court.

If Trump were to sell the Trump International Hotel in Washington -- or even transfer its ownership to his children -- the lawsuit likely would go away. Trump has kept his properties in a trust while he is in office.

The Justice Department has argued that Maryland and DC have no ability to sue and the case should be dismissed, and Trump's personal attorneys also say he can't be sued for this personally while he's President.

The two other cases include one in New York claiming Trump has an unfair business advantage, and one in DC federal court claiming Democrats in Congress should be able to review the President's business interests. Those have yet to reach a second round of arguments in front of a full appellate court, as this one has, making Thursday's arguments historic.

"He can be removed from office ... or he can be voted out of office. But to sue the president is a matter that is unplowed ground, and under the structure of the Constitution, the Supreme Court has not been very kindly to that. Now we have this district court that says we can sue the president," said Judge Paul Niemeyer. He had written an opinion dismissing the case previously.

"What's being asked here is wholly unprecedented. We have no history to guide us," Wilkinson said. "Congress has just been left on a back doorstep to freeze in the cold."

But another judge on the bench Thursday, Robert King, used the history of the Constitution to slam Trump. "He said they were 'phony,' " King said repeatedly, raising his voice as he cited Trump's tweets about the Emoluments Clause. "They were written in Philadelphia" at the Constitutional Convention of 1787, he added.

The Justice Department lawyer, Hashim Mooppan, responded, "He's calling the claims here phony. It's either a tweet or an off-the-cuff statement."

The early stage of the case didn't stop many of the judges from pushing for answers about what ultimately they could do about Trump's business interests.

Wilkinson asked the attorneys challenging Trump to tell him the goal of the case, describing how when you buy a ticket for a flight, you know where the plane will land.

"We've gotten through TSA," said Loren AliKhan, representing DC and Maryland.

The purpose of litigation is that you don't know where a plane will land, and courts must help decide, another judge, Albert Diaz, chimed in.

4th US Circuit Court of Appeals emoluments hearing in Richmond, Virginia.

Nearly all of the judges asked questions, with all but one or two appearing to reveal their thoughts on the case. Eight of the judges on the panel were appointed by Democratic presidents and seven by Republicans. Three judges appointed by Trump sat on the panel Thursday.

Early in the arguments, a quartet of female judges -- Diana Gribbon Motz, Barbara Milano Keenan, Pamela Harris and Stephanie Thacker -- harshly questioned Mooppan about legal technicalities he used to defend the President.

Motz, especially, voiced her agreement with the trial-level judge, Peter Messitte of Maryland, on the case.

"It's no slap-dash opinion," she said Thursday.

Almost two hours later, as Mooppan grew more passionate and repeatedly described his opponent, AliKhan, of the DC attorney general's office, simply as "she," Motz cut in to ask him to call her "colleague" or "counsel."

Previously, a smaller group of three judges, including a senior judge who did not sit on the panel Thursday, chose to dismiss the case, to Trump's delight. But the full appeals court then revived it.

This story has been updated with additional details from the hearing.