Despite the discovery of animal coronaviruses related to SARS-CoV-2, the evolutionary origins of this virus are elusive. We describe a meta-transcriptomic study of 411 bat samples collected from a small geographical region in Yunnan province, China, between May 2019 and November 2020. We identified 24 full-length coronavirus genomes, including four novel SARS-CoV-2-related and three SARS-CoV-related viruses. Rhinolophus pusillus virus RpYN06 was the closest relative of SARS-CoV-2 in most of the genome, although it possessed a more divergent spike gene. The other three SARS-CoV-2-related coronaviruses carried a genetically distinct spike gene that could weakly bind to the hACE2 receptor in vitro. Ecological modeling predicted the co-existence of up to 23 Rhinolophus bat species, with the largest contiguous hotspots extending from South Laos and Vietnam to southern China. Our study highlights the remarkable diversity of bat coronaviruses at the local scale, including close relatives of both SARS-CoV-2 and SARS-CoV. Display omitted •Four novel SARS-CoV-2-related viruses were identified in rhinolophid bats•RpYN06 is the closest relative of SARS-CoV-2 in most of the virus genome•A high diversity of bat coronaviruses was present in a very small geographic area•Ecological modeling reveals a broad range of rhinolophid bats in parts of Asia A study of 411 bat samples collected in Yunnan province, China between 2019 and 2020 yields 24 full-length coronavirus genomes, including four viruses highly related to SARS-CoV-2 and three to SARS. The closest relative to SARS-CoV-2 infects a species of bats that is found in regions that extend from South Laos and Vietnam to southern China.