Salmonella enterica serovar Minnesota (S. Minnesota) is an emerging serovar that persists within poultry supply chains, potentially causing outbreaks in humans. Understanding its population genomics is crucial for designing preventive measures. We performed a genomic surveillance study of S. Minnesota by analyzing 259 isolates from poultry in Saudi Arabia. Whole-genome sequencing data for these isolates were analyzed to characterize emerging clones and the genetic factors underlying antimicrobial resistance and virulence. We compared the isolates to all available global genomes of S. Minnesota. Our results revealed the emergence of four clones, three of which were mixed with global strains. These clones exhibited higher levels of antimicrobial resistance and virulence due to the acquisition of multiple plasmids, particularly IncC plasmids, carrying resistance and virulence genes. IncC plasmids underwent genomic rearrangements, presenting diverse configurations of resistance genes. Our findings demonstrate the emergence and persistence of pathogenic and multidrug-resistant S. Minnesota clones.