The H3N2 canine influenza virus (CIV) originated from an avian species. Since its emergence, it has circulated in multiple states and has caused pandemics among dog populations; however, no comprehensive studies have explored the causes driving these ongoing cases. The study of the codon usage patterns of viruses can reveal the genetic changes required for the viruses to adapt to new hosts and the external environment. Here we performed a thorough genetic, evolutionary, and codon usage analysis. We identified three evolutionary H3N2 CIV clades from a timescaled phylogenetic tree, namely, Origin, China, and Korea/USA, by principal component analysis (PCA). Additionally, we found a low codon usage bias and that mutation pressure, natural selection, and dinucleotide abundance shape the codon usage bias of H3N2 CIVs, with natural selection being more crucial than the others. Moreover, the human codon adaptation index was similar to that of dogs (the natural host) and cats. In addition, the H3N2 CIV similarity index values were higher than those of the avian influenza virus (AIV), suggesting viral adaptation to the host. Therefore, H3N2 CIVs may pose a potential risk to public health in the future, and further epidemiologic, evolutionary, and pathogenetic studies are required.