The Islamic republic shut its mosques and shrines in March as part of its efforts to contain the Middle East's deadliest outbreak of the novel coronavirus.
The reopening was granted for Laylat al-Qadr -- a high point during the fasting month of Ramadan that marks when the Koran was revealed to Prophet Mohammed.
But Health Minister Saeed Namaki sounded a note of caution as he announced that worshippers would be allowed to attend mosques and ceremonies for three of the next five nights.
"The biggest strategic mistake is to think that coronavirus is finished," he said in remarks broadcast on state television.
"At any time, we can go back to bad circumstances" due to "negligence", said Namaki.
"Our priority is to hold ceremonies outdoors" such as "in stadiums", he said, "so that social distancing is properly observed."
Namaki said his ministry agreed in a meeting to help "organise ceremonies from midnight to 2:00 am during the nights of Qadr".
He said the move came in response to "concern" expressed by Ayatollah Ali Khamenei, but stressed the supreme leader "always supports all measures" to contain the virus.