The recency of large-scale land conversion in California’s San Joaquin Desert raises the probability that the region’s numerous endemic species still retain genetic signatures of historical population connectivity. If so, genomic data can serve as a guidance tool for conserving lands that once supported habitat for gene movement. We studied the genetic structuring of the endangered blunt-nosed leopard lizard Gambelia sila, a San Joaquin Desert endemic, to (1) test whether patterns of population admixture could be used to delimit former habitat corridors in the pre-converted landscape, (2) evaluate whether restriction site associated DNA sequencing (RADseq) from a subset of samples can resolve structure at the same spatial scale as mtDNA and microsatellite data collected on the full sample, and (3) inform recovery efforts lacking direction from genetics. Cluster and tree-based analyses reveal a recent shared history between many populations that are now isolated, and that contemporary structure is linked to geophysical features that influence precipitation patterns and locations of former suitable habitat. Past hybridization with the sister species Gambelia wislizenii in southern San Joaquin Desert has generated a stable, but now-isolated population with different species identities for the mtDNA and nuclear genomes. The three marker types converged on similar themes, despite substantially fewer samples in the RADseq datasets; however, RADseq inferences were sensitive to dataset assembly filters that account for sequencing error, particularly cluster assignments. We suggest ways in which these data can be used to improve recovery efforts for G. sila and offer guidelines for RADseq dataset assembly in studies of intraspecific population structure.