SummaryPlumage color can be considered as a social signal in chickens and a breeding identification tool among breeders. The relationship between plumage color and trait groups of immunity, growth and fertility is still a controversial issue. This research aimed to determine the genome‐wide additive and epistatic variants affecting plumage color variation in chickens using the chicken Illumina 60k high‐density SNP array. Two scenarios of genome‐wide additive association studies using all SNPs and independent SNPs were carried out. To perform epistatic association analysis, the LD pruning approach was used to reduce the complexity of the analysis. We detected seven novel significant loci using all of the SNPs in the model and 14 SNPs using the LD pruning approach associated with plumage color. Moreover, 89 significantly associated SNP–SNP interactions (P‐value <10−6) distributed in 25 chromosomes were identified, indicating that all of the signals together putatively influence the quantitative variation of plumage color. By annotating genes relevant to top SNPs, we have distinguished 18 potential candidate genes comprising HNF4beta, CKMT1B, TBC1D22A, RPL8, CACNA2D1, FZD4, SGMS1, IRF8, OPTN, LOC420362, TRABD, OvoDA1, DAD1, USP6, RBM12B, MIR1772, MIR1709 and MIR6696 and also 89 putative gene–gene combinations responsible for plumage color variation in chickens. Furthermore, several KEGG pathways including metabolic pathway, cytokine–cytokine receptor interaction, focal adhesion, melanogenesis, glycosaminoglycan biosynthesis–keratan sulfate and sphingolipid metabolism were enriched in the gene‐set analysis. The results indicated that plumage color is a highly polygenic trait which, in turn, can be affected by multiple coding genes, regulatory genes and gene–gene epistasis interactions. In addition to genes with additive effects, epistatic genes with tiny individual effect sizes but significant effects in a pair have the potential to control plumage coloration in chickens.