We report on the phenotypic, molecular phylogenetic and pathogenic characterization of a novel azuki bean (Vigna angularis) root-rot (BRR) pathogen from Hokkaido, Japan, which formally is described herein as Fusarium azukicola. This species can be distinguished phenotypically from the other Phaseolus/Vigna BRR and soybean sudden-death syndrome (SDS) pathogens by the production of wider and longer four-septate conidia cultured on SNA. Molecular phylogenetic analyses of four anonymous intergenic loci, a portion of the translation elongation factor (EF-1α) gene and the nuclear ribosomal intergenic spacer region (IGS rDNA) strongly support the genealogical exclusivity of F. azukicola with respect to the other soybean SDS and BRR pathogens within Clade 2 of the F. solani species complex (FSSC). Evolutionary relationships of F. azukicola to other members of the SDS-BRR clade, however, are unresolved by phylogenetic analyses of the individual and combined datasets, with the exception of the IGS rDNA partition, which strongly supports it as a sister of the soybean SDS pathogen F. brasiliense. A multilocus genotyping assay is updated to include primer probes that successfully distinguish F. azukicola from the other soybean SDS and BRR pathogens. Results of a pathogenicity experiment reveal that the F. azukicola isolates are able to induce root-rot symptoms on azuki bean, mung bean (Vigna radiata), kidney bean (Phaseolus vulgaris) and soybean (Glycine max), as well as typical SDS foliar symptoms on soybean. Our hypothesis is that F. azukicola evolved in South America and was introduced to Hokkaido, Japan, on azuki bean but its possible route of introduction remains unknown.