Escherichia coli ST58 has emerged in recent years as a globally disseminated uropathogen that often progresses to sepsis. Unlike most pandemic (ExPEC) which belong to pathogenic phylogroup B2, ST58 is unusual as it belongs to the environmental/commensal phylogroup B1. Little is known about its evolution and emergence as a pathogen. To address this, we performed a pan-genomic analysis of a global collection of 752 ST58 genomes using a variety of microbial bioinformatics tools. Phylogenomic methods identified a large sub-lineage of ST58 comprising over half the sequences under investigation and the vast majority of infectious isolates. Gene screening revealed that nearly all members of this sub-lineage carried ColV plasmids, an important family of mobile genetic elements, which encode a variety of virulence factors that also promote intestinal fitness. A pan-genome wide association study (pan-GWAS) identified a variety of other acquired genomic traits that were strongly associated with this sub-lineage including the yersiniabactin genomic island, which also has important roles in virulence and gut fitness. Complementary analysis of 34,364 E. coli genomes from Enterobase revealed that whilst ColV plasmids feature in 16% of ExPEC across the species, they are primarily distributed in E. coli from food production animals, particularly poultry (55%) and pigs (20%). These observations implicate food production in the evolution of the major sub-lineage of ST58. Our work demonstrates that larger scale genomic investigations in conjunction with emerging bioinformatic tools can facilitate greater understanding of emerging microbial pathogens.