Extended-spectrum -lactamase-producing (ESBL-EC) strains present a significant menace to the well-being of both animals and humans. However, limited information is available regarding their profiles in pigeons. Using a combination of whole genome sequencing, drug susceptibility testing, and bioinformatics analysis, we examined the genomic features and epidemiology of 95 ESBL-EC strains (41 racing and 54 meat pigeons) that were isolated from 11 Chinese cities. These strains belonged to seven phylogenetic groups (A, B1, B2, C, D, E, and F). Moreover, these isolates have 51 serotypes, including several pathogenic ones (e.g., O51, O8, O4, O25, and O6). Notably, two high-risk clones, ST131 O25:H4, were found in racing pigeons and were responsible for the worldwide outbreaks of highly pathogenic and multidrug-resistant (MDR) infections. In addition, we found 41 multilocus sequence typing types, of which the dominant types were ST155, ST20, ST1011, and ST1196. In total, 91 isolates (95.79%) showed MDR, while eight isolates (8.42%) showed resistance to up to eight classes of antibiotics. Furthermore, we identified a series of ESBL genes in these isolates, including , , , , and . Also, 50 other antibiotic resistance genes (ARGs) were accompanied by the carriage of 33 plasmid replicon types, facilitating the horizontal spread of ARGs. Interestingly, three , four , and one (X4) were found in isolates of meat pigeons, and it was possible to successfully transfer the plasmids containing (X4) and to C600. In summary, this work presents the complexity of MDR profiles, plasmid profiles, and multiple typing profiles of Chinese ESBL-EC isolates of pigeon origin for the first time. The thorough investigation of ESBL-EC in pigeons presented in this work suggests that racing and meat pigeons are significant ARGs reservoirs.