Pectobacterium species, pectolytic necrotrophs, are responsible for devastating soft rot and blackleg diseases which lead to significant economic losses mainly on potato worldwide. The aim of this study was to reveal unknown genomic biology of all known species within the genus Pectobacterium through comparative genomic analyses. Numerous pseudogenes in P. carotovorum ssp. odoriferum suggest a low coding capacity and genomic degradation. Genome atlases showed distinct DNA structures and highlighted suspicious high transcription zones, possibly modulated by the nucleosome positioning. Orthologous analysis determined a pan and core genome sizes of 9,296 and 2,414 genes, respectively. Remarkable divergences were observed in gene clusters encoding pathogenicity determinants and antimicrobial compounds. Three distinct CRISPR-Cas systems, IF, IE and IIIA, were identified, with some species presenting both subtypes IF and IE. Additionally, a novel cellobiose phosphotransferase system was found exclusively in P. parmenteri, and an unreported T5SS is conserved in almost all species. Several virulence determinants, bactericide clusters and even a complete IIIA CRISPR-Cas system were predicted, confirming the horizontal gene transfer among the species. Our findings enhance understanding of how different species employ diverse mechanisms during the disease process and other important cellular functions.