Technical Abstract: 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 is formally 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 4-septate conidia cultured on synthetic nutrient agar(SNA). Molecular phylogenetic analyzes of four anonymous intergenic loci, a portion of the translation elongation factor (EF-1a) gene and the nuclear ribosomal intergenic spacer region (IGS rDNA) strongly supported 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, were unresolved by phylogenetic analyses of the individual and combined datasets, with the exception of the IGS rDNA partition which strongly supported it as a sister to the soybean SDS pathogen F. brasiliense. A previously published multilocus genotyping assay was updated to include primer probes that successfully distinguished F. azukicola from the other soybean SDS and BRR pathogens. Results of a pathogenicity experiment revealed that the F. azukicola isolates were 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 working 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.