The positive cases were identified out of roughly 13,800 tests. The new data raised the average rate of positive tests to 4.1 percent.
"It's another concerning data point," health department spokesperson Ben Truman said.
Franklin (72 cases), Lamoille (21 cases), and Rutland (74 cases) counties all set new records. Windsor, with 37 cases, tied its previous high.
But infections are distributed across the state. Chittenden County, Vermont's most populous, recorded 97 cases, the most in a day since the Delta variant arrived over the summer.
Before Thursday's numbers, Vermont's infection rate was already more than twice the national average, according to data compiled by the New York Times. Children under 11 have had the highest infection rate in Vermont in recent months, though they are far less likely to be hospitalized, state data show. Children ages 5-11 became eligible to get vaccinated last week.
Ongoing outbreaks include St. Michael's College in Colchester, where 87 students have become infected within the last two weeks, and the Northeast Correctional Complex in St. Johnsbury, where 23 prisoners and staff have tested positive.
There are currently 53 people hospitalized with COVID-19; 14 are in intensive care.
People who are not vaccinated against COVID-19 are more likely to be infected and to get seriously ill or die.
State officials have urged people to get vaccinated and wear masks indoors, but Gov. Phil Scott has consistently resisted pressure to turn his masking guidance into a mandate. He has said recently that his focus is on keeping the number of people who must be hospitalized for treatment to a level that does not overwhelm Vermont's health care system.
“If we make smart decisions in the coming weeks, and make an extra effort to protect the vulnerable, we can help reduce hospitalizations,” he said Tuesday at one of his weekly press conferences. “But it takes all of us committing to these smart, practical choices.”
That wasn't enough for the Democratic leaders of the Vermont House and Senate. Both sent statements later Thursday blasting Scott for failing to implement measures to slow the virus.
House Speaker Jill Krowinski (D-Burlington) called it "unfathomable to me that nothing is being done to address this unprecedented spread of the virus in every county in the state."
"The first thing that came to mind when I saw today’s case count of 591 was, ‘Why? Why is more action not being taken to protect Vermonters and keep our communities safe? Why don’t we implement the strategies we know work, like a mask mandate, to mitigate the spread of COVID-19?’" Krowinski wrote.
"The Governor has stated that he has the tools available to support our communities, but has yet to utilize those tools and has not articulated when the appropriate time is to roll out the mitigation strategies we know work," she continued.
"That time is now. That time was yesterday. That time was a month ago."
In a statement of her own, Senate President Pro Tempore Becca Balint (D-Windham) expressed frustration that her pleas for a change of course have been ignored for weeks.
"When things aren’t working, strong leaders do not stick their heads in the sand," she wrote. "They re-evaluate, pivot, and commit to a new path. This virus is unpredictable.
"We all hoped infection rates would drop as more Vermonters got vaccinated, but clearly that hasn’t happened, and we are overdue for a reassessment of strategy and a course correction," she continued. "It has to happen now. I look forward to talking with the administration about how to get this done.”
More than 60 people have died of COVID-19 since October 1.