Polymorphisms in the dopamine receptor D4 gene (DRD4) have been widely investigated to assess their correlation with variations in animal behavior. We precisely examined polymorphisms in the extracellular region of DRD4 in 75 avian species belonging to 16 orders and detected high degrees of polymorphism at inter- and intraordinal levels. The existence of a variable number of proline repeats (2 to 12 times) in the extracellular region was a common feature in all Neognathae, and a strong codon bias at synonymous sites was found among Passeriformes, Galliformes, and other non-passerine Neoaves. Furthermore, significantly higher values of the pairwise disparity index were detected in Passeriformes, suggesting either a substantial difference in the evolutionary processes or a higher level of mutation rate in the passerine clade. The differences in both codon bias and other genetic parameters among avian taxa would be explained by different levels of selective pressure on the extracellular region of DRD4. Our study suggested that different conformations determined in a sequence-dependent manner at the extracellular region could be one of the key factors affecting the efficiency and accuracy of DRD4 expression. Our findings further imply a possibility that behavioral diversity, which would be important during the processes of adaptive radiation, may be enhanced by the selection acting on indels or single-nucleotide substitutions in the extracellular region of DRD4.