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Dongxiang wild rice (DXWR) is one of the most valuable germplasm resources of rice. It is important to conserve the genetic diversity and uncover the population differentiation of DXWR. In this study, we analyzed the genetic diversity and population differentiation of DXWR based on whole-genome resequencing of 220 DXWR lines collected from nine natural populations in an ex situ conservation nursery. Almost half of the SNPs and Indels detected in these DXWR lines were absent in cultivated rice or other common wild rice, indicating the potential and importance of DXWR in rice breeding. Based on Structure and PCA analysis, these DXWR lines could be divided into two subpopulations, in which subpopulation G1 had more specific SNPs and Indels and was genetically more genetically diverse than subpopulation G2. The average Fst of regions with low relative genetic diversity between G1 and G2 were significantly lower than whole-genomic Fst, indicating directional selection in these regions. Some functional genes and QTLs were found to locate in highly differentiated regions between G1 and G2. Moreover, the deep root ratios of G2 were significantly higher than G1. Our results would be helpful to the conservation and utilization of DXWR germplasm.