The anatomically simple plants that first colonised land must have acquired molecular and biochemical adaptations to drought stress. Abscisic acid (ABA) coordinates responses leading to desiccation tolerance in all land plants. We identified ABA non-responsive mutants in the model bryophyte Physcomitrella patens and genotyped a segregating population to map and identify the ABA NON-RESPONSIVE (ANR) gene encoding a modular protein kinase comprising an N-terminal PAS domain, a central EDR domain and a C-terminal MAPKKK-like domain. anr mutants fail to accumulate dehydration tolerance-associated gene products in response to drought, ABA or osmotic stress, and do not acquire ABA-dependent desiccation tolerance. The crystal structure of the PAS domain, determined to 1.7A resolution, shows a conserved PAS-fold that dimerises through a weak dimerization interface. Targeted mutagenesis of a conserved tryptophan residue within the PAS domain generates plants with ABA non-responsive growth and strongly attenuated ABA-responsive gene expression, whereas deleting this domain retains a fully ABA-responsive phenotype. ANR orthologs are found in early-diverging land plant lineages and aquatic algae, but are absent from more recently diverged vascular plants. We propose that ANR genes represent an ancestral adaptation that enabled drought-stress survival of the first terrestrial colonisers, but were lost during land plant evolution.