President Cyril Ramaphosa says the National Coronavirus Command Council (NCCC) has decided that places of worship may resume services, but under strict conditions.
According to the president, the NCCC had recognised calls from religious leaders across the country, which is why faith-based organisations would now be allowed to congregate - under Level 3 regulations.
FULL SPEECH | Ramaphosa lifts ban on religious gatherings
The religious sector had fiercely lobbied to be allowed to gather, arguing that many people had been experiencing emotional and psychological distress due to the coronavirus outbreak and the lockdown. It had barred them from practising their faith at churches and from engaging with religious leaders.
In an address to the nation on Tuesday evening, Ramaphosa said places of worship could reopen from 1 June, when alert Level 3 kicks in. This is with strict restrictions, he added.
"Places of worship may open, subject to strict regulations," said Ramaphosa, using the occasion to reiterate a call for a day of national prayer.
"We recognise and appreciate their deep desire to return to their duties, to serve their communities and society," said Ramaphosa.
He said churches were now allowed to gather, but it would have to do so under the conditions of the Level 3 regulations. It meant only 50 people were allowed to congregate, depending on the space available.
"Our faith communities must ensure that any religious rituals that carry even the slightest possibility of exposing worshippers to risk should be avoided, and that where they form an essential part of religious practice, that sanitisation is paramount."
The president said the lockdown had taken a toll on the country, saying many were anxious and fearful of both the pandemic and the future of the country.
"We understand the great importance that the closure of places of worship has had on members of the faith community and this has worsened the distress of communities, who are unable to worship in congregation," said the president.
"South Africans are people of deep faith; our faith has seen us through many dark times and has sustained us," he added.
Ramaphosa thanked the faith-based community, saying its leaders have stood by the government and provided encouragement in the battle against the spread of the coronavirus.
He said the values shared by the many in the religious sector had come to the fore, in spite of the lockdown curtailing most of its activities.
He said all recognised places of worship needed to ensure their congregants wore face masks and hygiene protocols had to be in place, including deep cleaning of the areas before and after services.
The president said religious rituals that exposed worshippers to risk should be avoided.
He thanked religious leaders for making their churches available as space to be used for school lessons, quarantining, screening and testing, as well as places of shelter for survivors of gender-based violence.
He said Level 3 of the lockdown demanded vigilance from everyone in the country.
Sunday will be the day of national prayer.