Lawyers for the US state of Maryland and the capital Washington accused President Donald Trump on Monday of accepting illegal payments from foreign officials through his hotel in the US capital.
But a lawyer representing the president contended that such payments are perfectly legal, as long as Trump does not offer anything in return.
The lawsuit being heard in a Greenbelt, Maryland court revolves around the "emoluments clause" of the US constitution which prevents any public officer holder from accepting "any present, Emolument, Office, or Title, of any kind whatever, from any King, Prince, or foreign State" without the approval of the legislature.
The plaintiffs say Trump is guilty of having conflicts of interest, and has not sufficiently distanced himself from his businesses.
After becoming US president in January 2017, the real estate magnate entrusted his two sons with running his commercial interests, but retained all his shares in the Trump Organization.
The result has been that foreign dignitaries seeking to curry favor with the White House have chosen to stay at Trump International Hotel, according to Karl Racine, the attorney general for Washington and his counterpart for Maryland, Brian Frosh.
The debates on Monday attempted to define the concept of emoluments and what the framers of the constitution intended the clause when it was drafted in the 18th century.
There has never been a major case involving the arcane clause, and it has never been examined by the Supreme Court.
As a result, Monday's hearing was the "first oral argument focused on the meaning of the emoluments clause in American judicial history," according to Norm Eisen of anti-corruption group Citizens for Responsiblity and Ethics in Washington (CREW).
Commenting on the Department of Justice's position, which states that Trump is not guilty of violating the clause because he did not explicitly offer a quid pro quo, Eisen added: "Our view is that this is way too narrow.
"That's not how founders defined emoluments, not how US government has generally defined it, and makes no sense as matter of logic, would permit too much corruption."
Federal Judge Peter Messitte is expected to give his ruling by the end of July.