When rare plants are distributed across a range of habitats, ecotypic differentiation may arise requiring customized conservation measures. The rate of local adaptation may be accelerated in complex landscapes with numerous physical barriers to gene flow. In such cases, examining the distribution of genetic diversity is essential in determining conservation management units. We investigated the distribution of genetic diversity in the federally threatened Camissonia benitensis (Onagraceae), which grows in two distinct serpentine habitats across several watersheds in San Benito, Fresno, and Monterey Cos., CA, USA. We compared genetic diversity with that of its two widespread relatives, C. contorta and C. strigulosa, and examined the potential for hybridization with the latter species. Genotyping results using seven heterospecific microsatellite markers indicate that differentiation between habitat types was weak (F ST = 0.0433) and in an AMOVA analysis, there was no significant partitioning of molecular variation between habitats. Watersheds accounted for 11.6 % of the molecular variation (pairwise F ST = 0.1823–0.4275). Three cryptic genetic clusters were identified by InStruct and STRUCTURE that do not correlate with habitat or watershed. C. benitensis exhibits 5–11× higher inbreeding levels and 0.54× lower genetic diversity in comparison to its close relatives. We found no evidence of hybridization between C. benitensis and C. strigulosa. To maximize conservation of the limited amount of genetic diversity in C. benitensis, we recommend mixing seed representing the three cryptic genetic clusters across the species’ geographic range when establishing new populations.