is an opportunistic pathogen linked to outbreaks in powdered infant formula (PIF), primarily causing meningitis and necrotizing enterocolitis. Whole-genome sequencing (WGS) was used to characterize 18 strains isolated from PIF (powdered infant formula) manufacturing plants (2011-2015). Sequence Type (ST) 1 was identified as the dominant sequence type, and all isolates carried virulence genes for chemotaxis, flagellar motion, and heat shock proteins. Multiple antibiotic resistance genes were detected, with all isolates exhibiting resistance to Cephalosporins and Tetracycline. A significant correlation existed between genotypic and phenotypic antibiotic resistance. The plasmid was identified in the isolates recovered from the same PIF environment. All isolates harbored at least one intact phage. All the study isolates were compared with a collection of 96 publicly available genomes to place these isolates within a global context. This comprehensive study, integrating phylogenetic, genomic, and epidemiological data, contributes to a deeper understanding of outbreaks. It provides valuable insights to enhance surveillance, prevention, and control strategies in food processing and public health contexts.