The Chinese indigenous Shiqi (SQ) pigeon and the imported White King (WK) pigeon are two meat-type pigeon breeds of economical and nutritional importance in China. They displayed significant differences in such meat quality traits as intramuscular fat (IMF) content and fatty acid (FA) compositions in the breast muscles. In this study, we aimed to screen candidate genes that could affect fat-related meat quality traits in meat-type pigeons. We investigated the polymorphic variations at the genomic level using double-digest restriction-associated DNA (ddRAD) sequencing in 12 squabs of SQ and WK pigeons that exhibited significant inter-breed differences in IMF content as well as FA and amino acid compositions in the breast muscles, and screened candidate genes influencing fat-related traits in squabs through gene ontology analysis and pathway analysis. By focusing on 6019 SNPs, which were located in genes with correct annotations and had the potential to induce changes in the encoded proteins, we identified 19 genes (ACAA1, ACAA2, ACACB, ACADS, ACAT1, ACOX3, ACSBG1, ACSBG2, ACSL1, ACSL4, ELOVL6, FADS1, FADS2, HACD4, HADH, HADHA, HADHB, MECR, OXSM) as candidate genes that could affect fat-related traits in squabs. They were significantly enriched in the pathways of FA metabolism, degradation, and biosynthesis (p < 0.05). Results from molecular docking analysis further revealed that three non-synonymous amino acid alterations, ACAA1(S357N), ACAA2(T234I), and ACACB(H1418N), could alter the non-bonding interactions between the enzymatic proteins and their substrates. Since ACAA1, ACAA2, and ACACB encode rate-limiting enzymes in FA synthesis and degradation, alterations in the enzyme–substrate binding affinity may subsequently affect the catalytic efficiency of enzymes. We suggested that SNPs in these three genes were worthy of further investigation into their roles in explaining the disparities in fat-related traits in squabs.