Phyllosticta spp. are important pathogens of citrus plants. Several Phyllosticta species associated with Citrus species grown in China have been reported; however, the relative prevalences of individual species and the distributions of their genotypes among host Citrus species remain largely unknown. In this study, we conducted an extensive survey of Phyllosticta species across 11 citrus-producing provinces in southern China. From fruits and leaves with black spots or black-spot-like symptoms, a total of 461 Phyllosticta strains were isolated. Based on molecular (ITS, actA, tef1, gapdh, LSU, and rpb2 sequences) and morphological data, the strains were systematically identified as belonging to five species: P. capitalensis, P. citrichinaensis, P. citriasiana, P. citricarpa, and P. paracitricarpa. To further understand intraspecific genetic diversity and relationships, strains of five species from different geographic and host sources were analyzed based on the multilocus sequence data. Our population genetic analyses revealed that all five Phyllosticta species on citrus showed evidence for clonal dispersals within and among geographic regions. In addition, pathogenicity tests using representative strains showed that all five species can cause disease on the tested Citrus spp. We discuss the implications of our results for the control and management of Citrus Black Spot and related diseases.