Since 2000 the Central Methodist Church has cared for around 30,000 people who had fled to the country for safety.
But now the church is closing its doors to them and forcing them to find new accommodation.
Bishop Paul Verryn who initially opened the project 15 years ago said many in the church "had wanted the refugees to leave a long time ago".
He left his post on Wednesday but insists he was not forced out.
He told Al Jazeera: "I don't think everyone at the church had welcomed this project to allow refugees to live here."
"I don't think we can ever get away from the responsibility the faith communities have towards the needs of the vulnerable, [but] they have been antagonistic towards the project."
Evections of the refugees begun on New Year's Eve but it's thought some still remain in the church.
Most of the people seeking shelter there come from a number of African countries but particularly Zimbabwe.
They were offered food, a bed, counselling, medical services and education but that will now end.
The Bishop added: "We have a country that is fairly unfriendly to refugees. We have a cold prejudice towards them ... it's been a very difficult journey for many."
This was because many South Africans also needed help, he said.
Bishop Verryn said his church has fought against the anti-refugee feeling "over the past decade and it cost us dearly".
There are calls for the South African government to set up an alternative.