Potato common scab is an important bacterial disease afflicting potatoes around the world. Better knowledge of the local Streptomyces spp. populations causing this disease is key to developing durable control strategies. In this study, we isolated 230 Streptomyces strains from scab-infected potato tubers harvested from commercial potato fields located across the province of Quebec, Canada. The genetic diversity of this collection was first studied using repetitive element-based PCR fingerprinting, and the genomes of 36 representative strains were sequenced using PacBio’s sequencing technology. This enabled us to identify the strains to the species level, to study the distribution of previously characterized virulence-associated genes and clusters, and to explore the repertoires of putative plant cell wall-degrading enzymes. In parallel, the virulence of the 36 strains was evaluated using a potato tuber slice assay. The diversity was higher than previously reported, as eleven phytopathogenic species were found across the province. Among them, S. scabiei and S. acidiscabies were the most abundant as well as the most virulent. Strains belonging to these two species harbored numerous virulence determinants, including the thaxtomin biosynthetic gene cluster. By contrast, most weakly virulent strains lacked this cluster but harbored at least one known virulence determinant. The results obtained suggest that a higher number of virulence-associated genes and clusters in the genome of phytopathogenic Streptomyces spp. is associated with greater virulence. This study contributes to increasing the publicly available genomic resources of scab-causing Streptomyces spp., and expand our knowledge on the diversity and virulence of this important bacterial pathogen.