As global temperatures increase, understanding the genomic basis of plant adaptability to extreme environments and tolerance to abiotic stresses, especially heat and drought, has a major role to optimize productivity and survival of crops and other important plant species. Prior studies have shown that several species in a group of native California plants in the genus Boechera can survive longer than their closely related model species, Arabidopsis thaliana, under environmental extremes. The two species of interest in this study include Boechera arcuata, found in low-elevation coastal areas, and Boechera perrenans, found in desert and inland chaparral regions. To elucidate the molecular level of their adaptations to diverse environments and more specifically to desert conditions, we first generate chromosome-level genome assemblies and annotations of the two Boechera species and then integrate comparative and functional genomics approaches. Based on our results, a total of 47.5% and 44.7% of the assemblies contain repeat elements in B. arcuata and B. perennans, respectively with recent TE amplifications and mostly LINE elements expansions in B. perennans. The results also identify 1505 specific genes in B. arcuata and 1531 specific genes in B. perennans and reveal relatively conservation of synteny. Functional analysis of the species-specific genes provides substantial evidence of specific over-enriched GO terms related to photosynthesis in B. perennans. Collectively, these results will be used to find the evidence of transposon-mediated evolution, especially for recent LINE insertions into gene regions contributing the adaption of B. perennans to the desert habitat. Moreover, identification of candidate gene families associated with survival under environmental extremes will provide the basis for analyzing the evolutionary history of each family. The integration of omic-scale information will ultimately help us in predicting evolutionary responses of various species to desertification and effective utilization of available knowledge for the management of stress tolerance in plants.