Cercospora kikuchii has long been considered the causal agent of Cercospora leaf blight (CLB) and purple seed stain (PSS) on soybean, but a recent study found C. cf. flagellaris associated with CLB and PSS in Arkansas (United States) and Argentina. Here, we provide a broader perspective on the distribution of C. cf. flagellaris on soybean and alternate hosts within the United States (Arkansas, Louisiana, Mississippi, Missouri, and Kansas). We used a multilocus phylogenetic approach with data from actin, calmodulin, translation elongation factor 1-α, histone 3, the internal transcribed spacer region of rDNA and the mating-type locus to determine that two species, C. cf. flagellaris (200 of 205 isolates) and C. cf. sigesbeckiae (five of 205 isolates), are associated with CLB and PSS in the United States. In our phylogenetic analyses, species-level lineages were generally well-supported, though deeper-level evolutionary relationships remained unresolved, indicating that these genes do not possess sufficient phylogenetic signal to resolve the evolutionary history of Cercospora. We also investigated the potential for sexual reproduction in C. cf. flagellaris in Louisiana by determining the frequency of MAT1-1/MAT1-2 mating-type idiomorphs within the Louisiana population of C. cf. flagellaris. Though the MAT 1-2 idiomorph was significantly more common in our collection, the presence of both mating types suggests the potential for sexual reproduction exists.