We studied the population genetic structure underlying the geographic variation in the structural color of the geotrupid dung beetle, Phelotrupes auratus, which exhibits metallic body colors of different reflectance wavelengths perceived as red, green, and indigo. These forms occur parapatrically in an area of Japan. The color variation was not related to variation in climatic factors. Using single-nucleotide polymorphisms (SNPs) from restriction-site associated DNA sequences, we discriminated five groups of populations (west/red, south/green, south/indigo, south/red, and east/red) by a combination of genetic clusters (west, south, and east) and three color forms. There were three transition zones for the color forms: two between the red and green forms were hybrid zones with steep genetic clines, which implies the existence of barriers to gene flow between regions with different colors. The remaining transition zone between the green and indigo forms lacked genetic differentiation, despite the evident color changes, which implies regionally specific selection on the different colors. In a genome-wide association study, we identified four SNPs that were associated with the red/green or indigo color and were not linked with one another, which implies that the coloration was controlled by multiple loci, each affecting the expression of a different color range. These loci may have controlled the transitions between different combinations of colors. Our study demonstrates that geographic color variation within a species can be maintained by nonuniform interactions among barriers to gene flow, locally specific selection on different colors, and the effects of different color loci.