The genetic architecture and domestication history of Chinese indigenous ducks, particularly those with distinct traits like the Longsheng duck (LSD), are not well characterized. This study used whole-genome resequencing data from 540 ducks across 30 populations to explore the genetic diversity and structure of these ducks. Our findings suggest extensive interspecific hybridization between mallard and spot-billed duck. Comparing with other Chinese ducks, LSD is a distinct breed with moderate genetic diversity. Selective signal analysis identified several key genes impacting neural development, fat metabolism, immunity, and circadian rhythms like SLC25A20 and PER2. These genes showed strong selective pressures that parallelled other domestication processes. Additionally, EDNRB2 was identified as a potential gene influencing the unique coloration of LSD's plumage, bill, and webbed feet, associated with distinct mutations in non-coding regions. Comparative analysis with other indigenous breeds further pinpointed genes associated with LSD-specific traits, including plumage color, reproductive capabilities, and fat deposition, such as MITF, SPATA2, EIF2S2, PLIN3, ATP1B1, and CCDC80. Our findings clarify the population genetics of Chinese indigenous ducks. They also highlight key genes and mutations that shape the unique characteristics of LSD. These insights pave the way for further research into the genetic resources and domestication patterns of Chinese ducks.