Bacterial chondronecrosis with osteomyelitis (BCO) impacts animal welfare and productivity in the poultry industry worldwide, yet it has an understudied pathogenesis. While Avian PathogenicEscherichia coli(APEC) are known to be one of the main causes, there is a lack of whole genome sequence data, with only a few BCO-associated APEC (APECBCO) genomes available in public databases. In this study, we conducted an analysis of 205 APECBCOgenome sequences to generate new baseline phylogenomic knowledge regarding the diversity ofE. colisequence types and the presence of virulence associated genes (VAGs). Our findings revealed the following: (i) APECBCOare phylogenetically and genotypically similar to APEC that cause colibacillosis (APECcolibac), with globally disseminated APEC sequence types ST117, ST57, ST69, and ST95 being predominate; (ii) APECBCOare frequent carriers of ColV-like plasmids that carry a similar set of VAGs as those found in APECcolibac. Additionally, we performed genomic comparisons, including a genome-wide association study, with a complementary collection of geotemporally-matched genomes of APEC from multiple cases of colibacillosis (APECcolibac). Our genome-wide association study found no evidence of novel virulence loci unique to APECBCO. Overall, our data indicate that APECBCOand APECcolibacare not distinct subpopulations of APEC. Our publication of these genomes substantially increases the available collection of APECBCOgenomes and provides insights for the management and treatment strategies of lameness in poultry.