The emergence and dissemination of Escherichia coli ST131 in the early 2000s is well-documented. This ST accounts for ~20% of extra-intestinal pathogenic Escherichia coli (ExPEC) infections globally and displays high levels of resistance to multiple antibiotics. However, the effect of the emergence of ST131 on the wider E. coli population remains unknown. Here we show that alleles dominant within the ST131 pangenome have increased in prevalence in human-associated E. coli over the last 20 years. We found that exchange of genetic material has been largely intra-phylogroup, with significant enrichment of ST131-associated alleles observed in phylogroup B2 between 2000 and 2014. This enrichment has occurred via core genome introgression and accessory genome recombination, suggesting that bacterial integration, rather than warfare, may play a larger role in governing population dynamics than previously thought. Quantitative genetic analyses revealed that twice as many nucleotide substitutions were introduce through inter-strain recombination that de novo mutation. If maintained this would lead to progressive convergence. Our results demonstrate how the temporal dynamics of the ExPEC landscape can potentially influence the genomic content of closely related E. coli populations that are not necessarily ExPEC themselves. We identify allelic exchange driven by MGEs capable of crossing the phylogroup recombination barrier, most likely influenced by the transmission of multidrug resistance regions and their accumulation in ST131. This work exemplifies how examining the wider context of a pandemic lineage pangenome can provide further insight to the evolutionary processes and genetic hallmarks of successful pathogens.