The effective protection and utilization of poultry resources depend on an accurate understanding of the genetic diversity and population structure. The breeding of the specialized poultry lineage “Yufen 1”, with its defined characteristics, was approved by the China Poultry Genetic Resource Committee in 2015. Thus, to investigate the relationship between the progenitor H line and other poultry breeds, the genetic diversity and population structure of “Yufen 1” H line (YF) were investigated and compared with those of 2 commercial chicken breeds, the ancestor breed Red Jungle Fowls, and 11 Chinese indigenous chicken breeds based on a whole-genome resequencing approach using 8,112,424 SNPs. The genetic diversity of YF was low, and the rate of linkage disequilibrium decay was significantly slower than that of the other Chinese indigenous breeds. In addition, it was shown that the YF population was strongly selected during intensive breeding and that genetic resources have been seriously threatened, which highlights the need to establish a systematic conservation strategy as well as utilization techniques to maintain genetic diversity within YF. Moreover, a principal component analysis, a neighbor-joining tree analysis, a structure analysis, and genetic differentiation indices indicated that YF harbors a distinctive genetic resource with a unique genetic structure separate from that of Chinese indigenous breeds at the genome level. The findings provide a valuable resource and the theoretical basis for the further conservation and utilization of YF.