In a recurring point of interest for the court as it questioned the government, Justice Brett Kavanaugh raised the question of the "risk" of a "creative prosecutor" using "vague" criminal statutes -- including obstruction and conspiracy, which Trump faces -- against any president if they can't claim immunity.

In response, Department of Justice attorney Michael Dreeben said the question about the risk is "very serious" and "obviously it is a question that this court has to evaluate." He argued there is a "balanced protection" with "accountability" for the presidency.

Both Kavanaugh and Justice Samuel Alito appeared skeptical of Smith's use of at least some of the conspiracy and fraud-related charges in the case against Trump. Alito said to Dreeben: "I don't want to dispute the particular application of that [conspiracy statute] to the particular facts here, but would you not agree that is a peculiarly open-ended statutory prohibition? And that fraud under that provision, unlike under most other fraud provisions, does not have to do -- doesn't require any impairment of a property interest?"

Dreeben responded: "It is designed to protect the functions of the United States government and it is difficult to think of a more critical function than the certification of who won the election."

Justice John Roberts began his line of questioning by raising concerns about the opinion issued by the D.C. Circuit Court of Appeals in their rejection of Trump's claims of immunity.

Roberts said the statement that "a former president can be prosecuted for his official acts because the fact of the prosecution means that the former president has allegedly acted in defiance of the laws" concerned him because "as I read it, it says a former president can be prosecuted because he's being prosecuted."

Roberts said such a position could put too much faith in the justice system to act non-politically and out of good faith, and he asked whether the Supreme Court should send the opinion back down to make clear to the circuit court that that is not the law.

Michael Dreeben, arguing for the government, responded that there are "layered safeguards" that protect against malicious prosecution.

"We are not endorsing a regime that we think would expose former presidents to criminal prosecution in bad faith, for political animus, without adequate evidence or politically driven prosecution that would violate the Constitution," Dreeben said.

Asked by Justice Clarence Thomas why previous presidents were not prosecuted for controversial actions, prosecutor Michael Dreeben said "this is a central question."

"The reason why there have not been prior criminal prosecutions is that there were not crimes," he said.

He said there are "layers of safeguards" that ensure that former presidents do not have to "lightly assume criminal liability for any of their official acts."

After about an hour of questioning, Trump's attorney concluded his presentation before the court and Department of Justice attorney Michael Dreeben, representing Smith's team, began his argument with a short opening statement followed by what is expected to be approximately an hour of facing questions.

Dreeben called Trump's immunity claim a "novel theory [that] would immunize former presidents for criminal liability for bribery, treason, sedition, murder and, here, conspiring to use fraud to overturn the results of an election and perpetuate himself in power."

"Such presidential immunity has no foundation in the Constitution," Dreeben said. "The framers knew too well the dangers of a king who could do no wrong."

-ABC News' Adam Carlson

As Smith's team has noted in arguing against Trump, the former president's lawyers during his second Senate impeachment trial said in very clear terms that they believed a president could in fact be criminally prosecuted by the Department of Justice -- the opposite of what his legal team is currently arguing.

"If my colleagues on this side of the chamber actually think that President Trump committed a criminal offense -- and let's understand, a high crime is a felony and a misdemeanor is a misdemeanor; the words haven't changed that much over time -- after he is out of office, you go and arrest him," one of his attorneys said in opening statements during his impeachment trial in 2021, shortly after Jan. 6.

"We have a judicial process in this country, we have an investigative process in this country, to which no former officeholder is immune,” Trump's attorney said then.

But now, facing federal charges related to Jan. 6, Trump's lawyers argue a president can only be prosecuted if he is impeached, convicted by the Senate and removed from office.

The Senate in his second impeachment trial acquitted, though a majority of lawmakers voted to convict him.

-ABC News' Katherine Faulders