When organisms encounter heterogeneous environments, selection may favor the ability of individuals to tailor their phenotypes to suit the prevailing conditions. Understanding the genetic basis of plastic responses is therefore vital for predicting whether susceptible populations can adapt and persist under new selection pressures. Here, we investigated whether there is potential for adaptive plasticity in development time in the quacking frog Crinia georgiana, a species experiencing a drying climate. Using a North Carolina II breeding design, we exposed 90 family groups to two water depth treatments (baseline and low-water) late in larval development. We estimated the contribution of additive and non-additive sources of genetic variation to early offspring fitness under both environments. Our results revealed a marked decline in larval fitness under the stressful (low-water) rearing environment, but also that additive genetic variation was negligible for all traits. However, in most cases we found significant sire-by-dam interactions, indicating the importance of non-additive genetic variation for offspring fitness. Moreover, sire-by-dam interactions were modified by the treatment, indicating that patterns of non-additive genetic variance depend on environmental context. For all traits, we found higher levels of non-additive genetic variation (relative to total phenotypic variation) when larvae were reared under stressful conditions, suggesting that the fitness costs associated with incompatible parental crosses (e.g. homozygous deleterious recessive alleles) will only be expressed when water availability is low. Taken together, our results highlight the need to consider patterns of non-additive genetic variation under contrasting selective regimes when considering the resilience of species to environmental change.