The carnage came on a day of bloodshed with a suicide bomber killing 25 people at a Shiite mosque in Kuwait and a suspected Islamist attacking a factory in France.
There was no immediate claim of responsibility for the Tunisian attack, but the Islamic State group, which marks June 29 as the first anniversary of its "caliphate" straddling Iraq and Syria, said it was behind the Kuwait bombing.
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Interior ministry spokesman Mohamed Ali Aroui told AFP the toll is "28 dead including tourists", without giving their nationalities.
Health ministry official Henda Chebbi told Mosaique FM radio that 12 people were hospitalised with various injuries.
"It was a terrorist attack" targeting the Marhaba Hotel, Aroui said.
"The assailant was killed," he added, without ruling out the possibility of more than one attacker.
Secretary of State for Security Rafik Chelly told Mosaique FM the gunman was a Tunisian student unknown to authorities.
"He entered by the beach, dressed like someone who was going to swim, and he had a beach umbrella with his gun in it. Then when he came to the beach he used his weapon," Chelly said.
The shooting was the worst in modern-day Tunisia and came just nearly three months after a March attack on the Bardo National Museum in Tunis killed 21 foreign tourists and a policeman.
IS claimed responsibility for the Bardo attack although Tunisia says it was carried out by an Algerian jihadist.
Gary Pine, a British holidaymaker, said today's shooting happened at around midday when the beach was thronged.
"Over to our left, about 100 yards or so away, we saw what we thought was firecrackers going off," Pine told Britain's Sky News television.
"Only when you could start hearing bullets whizzing around your ear do you realise it was something a lot more serious than firecrackers."
Pine said panic spread quickly and people scrambled for safety.
"There was a mass exodus off the beach," said Pine, adding he heard 20 or 30 shots.
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