Escherichia coli (E. coli) is a major cause of diarrheal disease, capable of moving between diverse hosts and environments. Colonisation factors (CFs), essential for host adherence, influence host range, but their evolutionary dynamics within E. coli populations are poorly understood. Analysing 79,025 E. coli genomes, we traced CF movement within and across lineages and pathotypes. While a small subset of CFs are linked to specific enterotoxigenic E. coli (ETEC) clusters, most CFs are broadly distributed across E. coli lineages and pathotypes, suggesting an important function across all E. coli. We discovered novel gene clusters encoding potential CFs, termed kappa-variants. CFs move across phylogenetically relevant clusters and sometimes between pathotypes from various hosts, likely facilitated by their frequent association with plasmids. These virulence factors may drive niche expansion and enhance gene exchange across ecological niches. Comprehensive genomic surveillance and a holistic approach are needed to mitigate the global burden of E. coli-mediated diseases.