We examined patterns of genetic variance and covariance in two traits (i) carbon stable isotope ratio δ13C (dehydration avoidance) and (ii) time to flowering (drought escape), both of which are putative adaptations to local water availability. Greenhouse screening of 39 genotypes of Arabidopsis thaliana native to habitats spanning a wide range of climatic conditions, revealed a highly significant positive genetic correlation between δ13C and flowering time. Studies in a range of C3 annuals have also reported large positive correlations, suggesting the presence of a genetically based trade-off between mechanisms of dehydration avoidance (δ13C) and drought escape (early flowering). We examined the contribution of pleiotropy by using a combination of mutant and near-isogenic lines to test for positive mutational covariance between δ13C and flowering time. Ecophysiological mutants generally showed variation in δ13C but not flowering time. However, flowering time mutants generally demonstrated pleiotropic effects consistent with natural variation. Mutations that caused later flowering also typically resulted in less negative δ13C and thus probably higher water use efficiency. We found strong evidence for pleiotropy using near-isogenic lines of FRIGIDA and FLOWERING LOCUS C, cloned loci known to be responsible for natural variation in flowering time. These data suggest the correlated evolution of δ13C and flowering time is explained in part by the fixation of pleiotropic alleles that alter both δ13C and time to flowering.