Threatened plants often exist in small, genetically depauperate populations, which may reduce their capacity for genetically based adaptation, increasing their extinction risk. Non-genetic variation, including epigenomic diversity (DNA methylation), may also be relevant for the persistence of threatened plants, yet epigenomics are rarely incorporated into conservation assessments. Here, we focused on four Leavenworthia (Brassicaceae) species that all have low genetic diversity, including one widespread species and one threatened species with little remaining genetic variation due to asexual reproduction. We grew individuals from several maternal lines and populations of each species, exposed them to well-watered or drought treatments, measured phenotypic traits, and analyzed variation in DNA methylation using whole-genome bisulfite sequencing. We addressed four specific questions: (1) In each species, how do phenotypic traits and epigenomic diversity vary among populations and in response to drought? (2) Do patterns of epigenomic variation correspond to phenotypic variation within a species? (3) How do these parameters differ among Leavenworthia species that differ in geographic range size? and (4) What are the implications for conservation? Phenotypic and epigenomic responses to environmental stress differed among species, with the extent of plasticity possibly related to the geographic range size of the species. The genetically homogenous, threatened species, L. exigua var. laciniata exhibited both significant patterns of phenotypic variation and distinct maternal line epigenotypes. Our results suggest that epigenomic variation may help promote the persistence of genetically depauperate threatened plants, highlighting its potential as a novel conservation target to reduce extinction risk.