WASHINGTON—The Supreme Court appeared ready Tuesday to allow a felon to sell his firearms collection, with justices across the ideological spectrum skeptical of government arguments that such transfers should be strictly limited.

The collection of nearly 20 guns—which includes three M1 rifles from World War II and the Vietnam War, along with several handguns and shotguns—belongs to Tony Henderson, a former U.S. Border Patrol agent in Florida who sold marijuana on the side until his 2006 arrest. Mr. Henderson, who didn’t use...