Moraxella catarrhalis is an established pathogen of the upper respiratory tract, causing severe morbidity and mortality worldwide. As yet, there is no licenced vaccine for the species, and knowledge of M. catarrhalis virulence factors, particular with relation to the organism’s epidemiology and genomic diversity, is still lacking. In this study, we examined the whole genome sequences of 97 M. catarrhalis strains and mined them for the virulence genes, bro, copB, dsbB, hag, hsdM, mcap, mclS, modM, olpA, ompCD, ompE, oppABCDF, tatABC, and uspA. We then constructed distance trees for the divergence of the gene alleles and performed a meta-analysis of the genes’ evolutionary patterns; evolutionary pressures on the genes were inferred by comparing synonymous to non-synonymous substitution ratios (dN/dS). These data were contrasted to the phylogeny of M. catarrhalis based on known sero-susceptibility cladistics determined by MLST allele subsets, and the relative evolutionary pressures on virulence genes compared to housekeeping genes were computed. It was found that the virulence genes of M. catarrhalis clustered into two clades corresponding to the sero-susceptibilities of the species. However, an unexpected finding was that even though there is more diversity in resistance genes in the SS clade compared to the SR clade, there is significantly more purifying pressure on the virulence genes of the former clade compared to the latter. Additionally, with the exception of b-lactamase, we show that horizontal transfer of these virulence genes is confined to between strains of each sero-susceptibility clade, and that the evolution of these resistance genes is predominantly genetic drift, as compared to lateral gene transfer. More analysis on the pan-genome of M. catarrhalis, particularly regarding SS strains is required to elucidate genomic and evolutionary trends of the organism.