Friday's suspension of the ban was a temporary one. Under the French legal system, the Conseil d'Etat (Council of State) can hand down an interim verdict before taking time to decide on the legality of the case.
The Conseil ruled that local authorities could restrict individual liberties only if there were a "proven risk" to public order.
"The emotions and concerns arising from the terrorist attacks, notably the one perpetrated in Nice on July 14, cannot suffice to justify in law the contested prohibition measure," it said.
It added that "the contested decree has ... brought a serious and manifestly illegal infringement on basic freedoms such as freedom to come and go, freedom of conscience and personal freedom."
The French Council of the Muslim Faith (CFCM) has welcomed the ruling, describing it as "a victory for common sense."
France has been embroiled in a pitched debate about swimsuits, with Prime Minister Manuel Valls saying that his country was locked in a "battle of cultures" and that the burkini represented the enslavement of women.
"We have to wage a determined fight against radical Islam, against these religious symbols which are filtering into public spaces," Valls told the country's leading broadcaster, BFM-TV.
At least two ministers have come out in opposition to the government's support of the burkini bans.
"To pretend that swimming veiled or bathing on a beach dressed is in itself threatening to public order and the values of the Republic is to forget that those (secular) values are meant to allow each person to safeguard their identity," Health Minister Marisol Touraine wrote on her website.
Education Minister Najat Vallaud-Belkacem, a Muslim, said she opposed burkinis but dismissed Valls' argument that the ban was a useful tool in France's fight against militants.
"There is no link between the terror attacks of Daesh and the dress of a woman on the beach," Vallaud-Belkacem said, using the Arabic acronym for the so-called "Islamic State."
Sarkozy takes hard line
Socialist President Francois Hollande struck a more measured tone, saying that life in society "presumes that each person conforms to the rules, and that there is neither provocation nor stigmatization."
But Hollande's likely contender for president in next year's election, conservative Nicolas Sarkozy, was unequivocal.
"The burkini is a political act, a militant act, a provocation," Sarkozy told Figaro magazine. "Women who wear it are testing the Republic."
His hardline stance was rejected by Harry Potter author J.K. Rowling in a tweet:
Most bans in southeast
The high court began hearing arguments Thursday from two nongovernmental organizations, the Human Rights League and an anti-Islamophobia group. Both sought to overturn a local court's decision in the southern town of Villeneuve-Loubet, near Nice, which upheld the ban on Islamic swimsuits.
However, some French town halls in the region, including that of Nice, have said they would maintain their bans on the burkini despite the ruling. A lawyer for Human Rights League, Patrice Spinosi, said that he would systematically take each case to court if they did not withdraw their orders.
On a visit to Paris on Thursday, London mayor Sadiq Khan, the first Muslim to be elected mayor of a Western capital, condemned the ban, saying no one should tell women what to wear.
"I don't think it's right," Khan told Britain's "Evening Standard" newspaper. "One of the joys of London is that we don't simply tolerate difference, we respect it, we embrace it."
tj,bik/kl (Reuters, AP, AFP, dpa)