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This study assessed the clonal diversity, the resistance profile and the virulence potential of Escherichia coli strains isolated from diabetic foot infection (DFI) and diabetic foot osteomyelitis (DFOM). A retrospective single-centre study was conducted on patients diagnosed with E. coli isolated from deep DFI and DFOM at Clinique du Pied Diabétique Gard-Occitanie (France) over a two-year period. Phylogenetic backgrounds, virulence factors (VFs) and antibiotic resistance profiles were determined. Whole-genome analysis of E. coli strains isolated from same patients at different periods were performed. From the two-years study period, 35 E. coli strains isolated from 33 patients were analysed; 73% were isolated from DFOM. The majority of the strains belonged to the virulent B2 and D phylogenetic groups (82%). These isolates exhibited a significant higher average of VFs number than strains belonging to other groups (p < 0.001). papG2 gene was significantly more detected in strains belonging to B2 phylogroup isolated from DFI compared to DFOM (p = 0.003). The most prevalent antibiotic resistance pattern was observed for ampicillin (82%), cotrimoxazole (45%), and ciprofloxacin (33%). The genome analysis of strains isolated at two periods in DFOM showed a decrease of the genome size, and this decrease was more important for the strain isolated at nine months (vs. four months). A shared mutation on the putative acyl-CoA dehydrogenase-encoding gene aidB was observed on both strains. E. coli isolates from DFOM were highly genetically diverse with different pathogenicity traits. Their adaptation in the bone structure could require genome reduction and some important modifications in the balance virulence/resistance of the bacteria.