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Summary Plant adaptation to a desert environment and its endemic heat stress is poorly understood at the molecular level. The naturally heat‐tolerant Brassicaceae speciesAnastatica hierochunticais an ideal extremophyte model to identify genetic adaptations that have evolved to allow plants to tolerate heat stress and thrive in deserts.We generated anA. hierochunticareference transcriptome and identified extremophyte adaptations by comparingArabidopsis thalianaandA. hierochunticatranscriptome responses to heat, and detecting positively selected genes inA. hierochuntica.The two species exhibit similar transcriptome adjustment in response to heat and theA. hierochunticatranscriptome does not exist in a constitutive heat ‘stress‐ready’ state. Furthermore, theA. hierochunticaglobal transcriptome as well as heat‐responsive orthologs, display a lower basal and higher heat‐induced expression than inA. thaliana. Genes positively selected in multiple extremophytes are associated with stomatal opening, nutrient acquisition, and UV‐B induced DNA repair while those unique toA. hierochunticaare consistent with its photoperiod‐insensitive, early‐flowering phenotype.We suggest that evolution of a flexible transcriptome confers the ability to quickly react to extreme diurnal temperature fluctuations characteristic of a desert environment while positive selection of genes involved in stress tolerance and early flowering could facilitate an opportunistic desert lifestyle.