Dehydration proteins (dehydrins, DHNs) confer tolerance to water-stress deficit to plants, thus playing a fundamental role in plant response and adaptation to water-deprivation stressful environments. We have performed a comparative genomics and evolutionary study of DHN genes in four model Brachypodium grass species, and a drought-induced functional analysis in 32 ecotypes of the flagship species B. distachyon, to gain insight into the origins and dynamics of these proteins and the correlated drought-mediated phenotypic responses in ecotypes showing different hydric requirements. Genomic sequence analysis detected 10 types of dehydrin genes (Bdhn) across the Brachypodium species, totalling 47 genes. Domain and conserved motif contents of peptides encoded by Bdhn genes revealed eight protein architectures, YSɸK2 being the most common architecture. Bdhn genes were spread across several chromosomes and more frequent in syntenic chromosomes 3 and 4 of B. distachyon, 4 and 5 of B. stacei and 4 of B. sylvaticum. Tandem and segmental duplication events were detected for four Bdhn genes. Selection analysis indicated that all the Bdhn genes were constrained by purifying selection. Three upstream cis-regulatory motifs (BES1, MYB124, ZAT) were consistently detected in several Bdhn genes. Functional analysis in 32 natural accessions of B. distachyon demonstrated that only four Bdhn genes (Bdhn1, Bdhn2, Bdhn3, Bdhn7) were expressed in mature leaves and that all of them were significantly more highly expressed in plants under drought conditions. These genes corresponded to wheat orthologs that were also significantly more expressed under drought stress. Brachypodium dehydrin expression was significantly correlated with drought-response phenotypic traits (plant biomass, leaf carbon and proline contents and WUE increases, leaf water and nitrogen content changes) being more pronounced in drought-tolerant ecotypes. Bdhn expression, associated phenotypic trait changes and climate niche variation did not show significant phylogenetic signal when tested in the B. distachyon genealogical-species tree. By contrast, some of them showed low or marginal significant phylogenetic signal when tested in the B. distachyon Bdhn tree, suggesting that Bdhn gene evolution is partially related to adaptation to drought in this species. Our results demonstrate that dehydrin composition and regulation is a key factor determining the acquisition of water-stress tolerance in grasses.