Rapidly decreasing water availability as a consequence of climate change is likely to endanger the range of long-lived tree species. A pressing question is, therefore, whether adaptation to drought exists in important temperate tree species like European beech (Fagus sylvatica L.), a wide-spread, dominant forest tree in Central Europe. Here, five beech stands were selected along a precipitation gradient from moist to dry conditions. Neutral genetic markers revealed strong variation within and little differentiation between the populations. Natural regeneration from these stands was transferred to a common garden and used to investigate the expression of genes for abscisic acid (ABA)-related drought signaling [9-cis-epoxy-dioxygenase (NCED), protein phosphatase 2C (PP2C), early responsive to dehydration (ERD)] and stress protection [ascorbate peroxidase (APX), superoxide dismutase (SOD), aldehyde dehydrogenase (ALDH), glutamine amidotransferase (GAT)] that are involved in drought acclimation. We hypothesized that progenies from dry sites exhibit constitutively higher expression levels of ABA- and stress-related genes and are less drought responsive than progenies from moist sites. Transcript levels and stress responses (leaf area loss, membrane integrity) of well-irrigated and drought-stressed plants were measured during the early, mid- and late growing season. Principal component (PC) analysis ordered the beech progenies according to the mean annual precipitation at tree origin by the transcript levels of SOD, ALDH, GAT and ERD as major loadings along PC1. PC2 separated moist and drought treatments with PP2C levels as important loading. These results suggest that phosphatase-mediated signaling is flexibly acclimated to the current requirements, whereas stress compensatory measures exhibited genotypic variation, apparently underlying climate selection. In contrast to expectation, the drought responses were less pronounced than the progeny-related differences and the transcript levels were constitutively lower in beeches from dry than from moist sites. These results imply that beeches from dry origins may have evolved mechanisms to avoid oxidative stress.