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, we designated 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.