In modern advanced genetics and breeding programs, the study of genes related to pigmentation in ducks is gaining much attention and popularity. Genes and DNA mutation cause variations in the plumage color traits of ducks. Therefore, discovering related genes responsible for different color traits and pigment patterns on each side of the single feathers in Chinese ducks is important for genetic studies. In this study, we collected feather images from 340 ducks and transported them into Image Pro Plus (IPP) 6.0 software to quantify the melanin content in the feathers. Thereafter, a genome-wide association study was conducted to reveal the genes responsible for variations in the feather color trait. The results from this study revealed that the pigmented region was larger in the male ducks as compared to the female ducks. In addition, the pigmented region was larger on the right side of the feather vane than on the left side in both dorsal and ventral feathers, and a positive correlation was observed among the feather color traits. Further, among the annotated genes, WNT3A, DOCK1, RAB1A, and ALDH1A3 were identified to play important roles in the variation in pigmented regions of the various feathers. This study also revealed that five candidate genes, including DPP8, HACD3, INTS14, SLC24A1, and DENND4A, were associated with the color pigment on the dorsal feathers of the ducks. Genes such as PRKG1, SETD6, RALYL, and ZNF704 reportedly play important roles in ventral feather color traits. This study revealed that genes such as WNT3A, DOCK1, RAB1A, and ALDH1A3 were associated with different pigmentation patterns, thereby providing new insights into the genetic mechanisms of single-feather pigmentation patterns in ducks.