Jiaji Duck (JJ) is a Muscovy duck species that possesses many superior characteristics, and it has become an important genetic resource in China. However, to date, its genetic characteristics and genetic relationship with other duck breeds have not been explored yet, which greatly limits the utilization of JJ. In the present study, we investigated the genome sequences of 15 individual ducks representing five different duck populations, including JJ, French Muscovy duck (FF), mallard (YD), hong duck (HD) and Beijing duck (BD). Moreover, we investigated the characteristics of JJ-specific single nucleotide polymorphisms (SNPs) and compared the genome sequences of JJ vs. YD and JJ vs. BD using integrated strategies, including mutation detection, selective screening, and Gene Ontology (GO) analysis. More than 40 Gb of clean data were obtained for each population (mean coverage of 13.46 Gb per individual). A total number of 22,481,367 SNPs and 4,156,829 small insertion-deletions (Indels) were identified for the five duck populations, which could be used as molecular markers in breeding and utilization of JJ. Moreover, we identified 1,447,932 JJ-specific SNPs, and found that genes covering at least one JJ-specific SNP mainly involved in protein phosphorylation and dephosphorylation, as well as DNA modification. Phylogenetic tree and principal components analysis (PCA) revealed that the genetic relationship of JJ was closest to FF, while it was farthest to BD. A total of 120 and 111 genes were identified as positive selection genes for JJ vs. BD and JJ vs. YD, respectively. GO and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses showed that the positive selection genes for JJ vs. BD ducks mainly involved in pigmentation, muscle contraction and stretch, gland secretion, and immunology, while the positive selection genes obtained from JJ vs. YD ducks mainly involved in embryo development, muscle contraction and stretch, and gland secretion. Taken together, our findings enabled us to better understand the characteristics of JJ and provided a molecular basis for the breeding and hybrid utilization of JJ in the future.