Population genomics can reveal cryptic biological diversity that may impact fitness while simultaneously serving to delineate relevant conservation units. Here, we leverage the power of whole-genome resequencing for conservation by studying 433 individual lesser prairie-chicken (Tympanuchus pallidicinctus; LEPC, a federally endangered species of conservation concern in the United States) and greater prairie-chicken (Tympanuchus cupido; GRPC, a legally huntable species throughout much of its range). The genomic diversity of two formally recognized distinct population segments (DPSs) of LEPCs is similar, but they are genetically distinct. Neither DPS is depleted of its genomic diversity, neither is especially inbred, and temporal diversity is relatively stable in both conservation units. Interspecific differentiation between the two species was only slightly higher than that observed between LEPC DPSs, due largely to bidirectional introgression. The high resolution provided by our dataset identified a genomic continuum between the two species such that individuals sampled from the hybrid zone were imperfectly assigned to their presumptive species when considering only their physical characteristics. The admixture between the two species is reflected in the spectrum of individual ancestry coefficients, which has legal implications for the “take” of individuals under the Endangered Species Act. Overall, our data highlight the recurring dissonance between static policies and dynamic species boundaries that are increasingly obvious in the population genomic era.