We sequenced and assembled genomes for 17 isolates of Staphylococcus cohnii isolated from osteomyelitis lesions in young broilers from two separate experiments where we induced lameness using a hybrid wire-litter flooring system. Whole genome comparisons using three different methods support a close relationship of genomes from both S. cohnii and Staphylococcus urealyticus. The data support three different lineages, which we designated as Lineage 1, Lineage 2, and Lineage 3, uniting these two species within an evolving complex. We present evidence for horizontal transfer between lineages of genomic regions from 50–440 kbp. The transfer of a 186 kbp region from Lineage 1 to Lineage 2 appears to have generated Lineage 3. Human-associated isolates appear to be limited to Lineages 2 and 3 but Lineage 2 appears to contain a higher number of human pathogenic isolates. The chicken isolates from our lameness trials included genomically diverse isolates from both Lineage 1 and 2, and isolates from both lineages were obtained from osteomyelitis lesions of individual birds. Our results expand the diversity of Staphylococci associated with osteomyelitis in poultry and suggest a high diversity in the microbiome of day-old chicks. Our data also support a reevaluation and unification of the taxonomic classifications of S. cohnii and S. urealyticus.