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SUMMARY Extreme dryness is lethal for nearly all plants, excluding the so‐called resurrection plants, which evolved vegetative desiccation tolerance (VDT) by recruiting genes common in most plants. To better understand the evolution of VDT, we generated chromosome‐level assemblies and improved genome annotations of twoSelaginellaspecies with contrasting abilities to survive desiccation. We identified genomic features and critical mechanisms associated with VDT through sister‐group comparative genomics integrating multi‐omics data. Our findings indicate thatSelaginellaevolved VDT through the expansion of some stress protection‐related gene families and the contraction of senescence‐related genes. Comparative analyses revealed that desiccation‐tolerantSelaginellaspecies employ a combination of constitutive and inducible protection mechanisms to survive desiccation. We show that transcriptional priming of stress tolerance‐related genes and accumulation of flavonoids in unstressed plants are hallmarks of VDT inSelaginella. During water loss, the resurrectionSelaginellainduces phospholipids and glutathione metabolism, responses that are missing in the desiccation‐sensitive species. Additionally, gene regulatory network analyses indicate the suppression of growth processes as a major component of VDT. This study presents novel perspectives on how gene dosage impacts crucial protective mechanisms and the regulation of central processes to survive extreme dehydration.