The hour-long argument brought a surprise: a question by Justice Clarence Thomas, and one that went in an opposite direction. He inquired about the race of jurors dismissed by defense lawyers for Curtis Flowers, drawing out the information that they were white.
Thomas is famous for remaining silent during oral arguments, and last asked a question three years ago.
Flowers has been accused and convicted of murdering four people - Bertha Tardy, Carmen Rigby, Robert Golden and Derrick Stewart - in July 1996 in a furniture store in Winona, Mississippi.
But two of his trials - the only ones in which more than one African American sat on the panel - resulted in hung juries. In three other trials, convictions were overturned because of misconduct on the part of District Attorney Doug Evans violated the Supreme Court's ruling in Batson v. Kentucky, which says that jurors may not be dismissed because of their race.
The Mississippi Supreme Court upheld Flowers' 2010 conviction, in which Evans struck five of six black potential jurors. It said he had race-neutral reasons for doing so.
Flowers' case has attracted the attention of national media, a television documentary and, recently, a celebrated podcast, all of which have raised questions about his innocence.
But Wednesday, the person in what became an unflattering spotlight was Evans, and the question for the court was whether it should ignore the past prosecutions and concentrate only on the 2010 trial.
Justice Samuel Alito, a conservative who usually is skeptical of criminal defendants, seemed the most likely to accept that Evans may have had legitimate reasons for the strikes in the 2010 trial.
Nevertheless, "the history of the case prior to this trial is very troubling," Alito said, adding "it is cause for concern and is certainly relevant to the decision that ultimately has to be made in the case."
Alito, Chief Justice John Roberts and others seemed to be searching for a rule that would guide courts about how far in the past they should go to judge whether a prosecutor's stated reasons for striking a juror are just.
Sheri Lynn Johnson, representing Flowers, said the court has made clear in past rulings that such history is relevant. She said there was no way to look at the record and miss Evans' motivations.
"The only plausible interpretation of all of the evidence viewed cumulatively is that Doug Evans began jury selection in [the 2010 trial] with an unconstitutional end in mind: to seat as few African American jurors as he could," she said.
Justices across the ideological spectrum seemed disturbed by what Justice Sonia Sotomayor called Evans' "passion" for prosecuting Flowers.
Justice Elena Kagan said the difference in how Evans questioned white potential jurors and black potential jurors was "staggering." In the 2010 trial, he asked 145 questions of the five black potential jurors he rejected, and only 12 inquiries to the 11 white jurors he seated.
One black juror he rejected said she strongly supported the death penalty, Kagan noted.
"Except for her race, you would think that this is a juror that a prosecutor would love when she walks in the door," Kagan said to Jason Davis, the special assistant attorney general representing Mississippi.
Davis acknowledged that the history of the case was "troubling" and the court must consider the history. But he said that in the most recent trial - "Flowers VI,'' the justices called it - the strikes could be justified.
When picking a jury, some potential panel members are eliminated by the judge and lawyers for cause - that they are likely to be biased, for instance, or because they say in a capital case that they could not impose the death penalty.
Prosecutors and defense attorneys also have what are known as peremptory challenges. They can strike potential jurors they simply don't want on the jury, and generally those choices cannot be second-guessed.
But in the 1986 Batson decision, the Supreme Court said the challenges could not be used to strike potential jurors because of their race. (Gender was later added as a forbidden purpose.)
In a more recent decision, the court said judges should consider the "totality of the circumstances" when deciding whether a prosecutor was using the challenges as a pretext for barring jurors because of their race.
Justice Brett Kavanaugh, who as a Yale law student wrote an article calling for tough enforcement of Batson, indicated that he did not think Evans lived up to the intent of the decision.
"Part of Batson was about confidence of the community and the fairness of the criminal justice system, right?" Kavanaugh asked Davis. "And that was against a backdrop of a lot of decades of all-white juries convicting black defendants."
In the last case where the Supreme Court said a prosecutor had violated Batson by striking black jurors, Thomas was the lone dissenter. He said courts in most cases should defer to the decisions made by trial judges.
His question indicated he might feel the same way in this case. Still, it was a surprise because he so rarely speaks during arguments.
Johnson acknowledged that Flowers's attorneys had struck white jurors, although she noted it was Evans' conduct that was being examined.
Sotomayor interjected that because of Evans' actions, white jurors were the only ones left to strike.
The case is Flowers v. Mississippi.
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