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Pectobacterium atrosepticum (Pba) are phytopathogenic, pectinolytic, non-sporulating, gram-negative rods causing blackleg and soft rot diseases in potato. They are ubiquitously present under temperate climate conditions and contribute to significant economic losses. Currently, there are no efficient control methods against soft rot Pectobacteriaceae (SRP). As limitation of the spread of SRP is solely prevention-based, we undertook broad characterization on both genotypic and phenotypic levels of the P. atrosepticum isolates acquired during monitoring of potato fields in Poland in 2013, 2014 and 2016. Of REP, ERIC and BOX-based genomic fingerprinting, the BOX-based approach turned out to be the most informative and allowed for classification of 118 Pba strains into six groups. The present study indicated that IV and I BOX profiles dominated among the investigated population. Finally, 23 Pba strains representing all BOX groups and originating from various growing seasons were selected for genotypic, phylogenetic and phenotypic studies. rpoS-based phylogeny revealed intraspecies variation (16 SNP sites) among the studied Pba strains, in contrast to the analyses relying on gyrA (1 SNP) and recA (0 SNP) sequences. Pba strains showed higher potency to macerate potato tissue at 20 °C than 28 °C. These isolates exhibited rather uniform production of plant cell wall degrading enzymes (pectinases, cellulases and proteases), lipases, siderophores and biofilm, however in the majority of cases inferior in comparison to Dickeya solani and Pectobacterium carotovorum strains. In conclusion, this study revealed genotypic and phenotypic uniformity in addition to high virulence potential of Pba strains isolated from potato fields during several growing seasons in Poland.