The case marks the first time the justices considered Section 3 of the 14th amendment.
During about two hours of arguments, Chief Justice John Roberts and the high court's other conservative justices peppered the lawyers representing Trump's challengers with a series of questions that suggested they were seeking a way to side with the former president - most likely based on reasoning that doesn't address the question of whether he is or isn't an insurrectionist.
Even some members of the court's liberal wing posed difficult questions to the lawyers opposed to the former president.
The case is the most significant elections matter the justices have been forced to confront since the Bush v. Gore decision in 2000 effectively handed the presidency to George W. Bush. If the Supreme Court ultimately rules against Trump it would almost certainly end his campaign for another term.
At issue is a provision in the 14th Amendment that bars certain public officials from serving in the government again if they took part in an insurrection. The voters who challenged Trump say his role in the January 6, 2021, attack on the US Capitol makes him ineligible under that "insurrection ban."
The Supreme Court often takes a few months to craft opinions - and usually hands down its biggest cases at the end of its term in June. But because the court expedited the earlier stages of the Trump ballot case, it is likely the court will want to move quickly to decide the case, potentially within a matter of weeks.
Here's what to know from Thursday's hearing:
Throughout the course of the arguments, the court's conservatives repeatedly questioned whether the insurrection ban was intended to apply to former presidents and whether the ban could be enforced without Congress first enacting a law. Others delved into more fundamental questions about whether courts removing a candidate from the ballot is democratic.
"Your position has the effect of disenfranchising voters to a significant degree," conservative Justice Brett Kavanaugh said in one of the more striking exchanges with attorneys.
If Trump is removed from the ballot in Colorado, Roberts predicted that states would eventually attempt to knock other candidates off the ballot. That, he signaled, would be inconsistent with the purpose and history of the 14th Amendment.
"It'll come down to just a handful of states that are going to decide the presidential election," Roberts said. "That's a pretty daunting consequence."
The amendment's key provision, Section 3, says in part: "No person shall ... hold any office ... under the United States ... who, having previously taken an oath ... to support the Constitution of the United States, shall have engaged in insurrection or rebellion against the same, or given aid or comfort to the enemies thereof."
One of the most notable line of questions came from Kavanaugh.
A 19th Century Supreme Court case, In Re. Griffin, involved a defendant's challenge to a criminal conviction based on the fact that the judge in the case had fought for the Confederacy. Chief Justice Salmon Chase, who was writing for an appeals court, ruled in 1869 that the "insurrectionist ban" could not be enforced against the judge unless Congress first passed a law.
Trump and his allies raised the case during their written arguments to the Supreme Court.
Kavanaugh repeatedly suggested that he believed the case offered important insight into the meaning of the insurrection ban. That would suggest that he, at least, is thinking about siding with Trump on the narrow grounds that states can't enforce the ban without Congress first passing legislation.
"It's by the chief justice of the United States a year after the 14th Amendment," Kavanaugh said in a reference to Chase. "That seems to me high probative of what the meaning or understanding of that otherwise elusive language is."
Another sign that the court was leaning toward Trump's position: Even some of the liberal justices posed difficult questions to the lawyers representing his challengers.
Notably, Justice Ketanji Brown Jackson, a Joe Biden nominee, said that the 14th Amendment provision did not include the word "president," even though it specifically listed other officials who would be covered, such as members of Congress. That is a central argument Trump's attorneys have raised in the case.
"They were listing people that were barred and 'president' is not there," Jackson said. "I guess that just makes me worry that maybe they weren't focused on the president."
Justice Elena Kagan questioned the implications of a single state banning a candidate in a presidential election.
"Why should a single state have the ability to make this determination not only for their own citizens, but for the rest of the nation?" Kagan asked.
All three of the court's liberal justices - Jackson, Sonia Sotomayor and Kagan - asked tough questions of both sides but they generally focused on narrow provisions, avoiding broad questions about whether the president engaged in an insurrection. Heading into the arguments, many experts predicted that would suggest the arguments were moving in Trump's direction.
The nine justices spent little time on the former president's actions surrounding the January 6 attack on the US Capitol that sparked the ballot challenge in Colorado and elsewhere.
There were more questions, in fact, about the Civil War and how the insurrectionist ban in the 14th Amendment of the Constitution was enacted in order to grapple with confederates who fought against the Union.
When Trump's attorney Jonathan Mitchell was questioned, none of the justices asked about whether Trump's actions constituted an insurrection until Jackson raised it in her final question.
"For an insurrection, there needs to be an organized concerted effort to overthrow the government of the United States through violence," Mitchell said when asked to explain his argument that Trump's actions did not involve an attempt to overthrow the government.
"So if point is that a chaotic effort to overthrow the government is not an insurrection?" the justice responded.
"This was a riot, it was not an insurrection," Mitchell responded.
Later, during questioning of Jason Murray, the attorney representing Colorado voters, Kavanaugh questioned why Trump should be removed from the ballot when he has not been convicted of inciting an insurrection. Kavanaugh noted there was a federal statute for insurrection and that Trump had not been charged with it, although he is facing other charges from special counsel Jack Smith related to his actions after the 2020 election.
Murray argued that the federal insurrection statute was enacted before the 14th Amendment was adopted, and that a federal conviction was not required to remove Trump from the ballot.
The provision does not say a conviction is necessary for disqualification, though some analysts have said a criminal conviction would help ensure that there was due process before anyone would be barred from office. After the Civil War, thousands of ex-Confederates were disqualified from office without prior criminal convictions.
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