Increasing climate variability is predicted to pose an even greater risk to species than climate warming. Using a series of common garden experiments, the influence of directional warming and increasing climate variability on marine stickleback phenotypic variation was investigated by simulating changes to the mean and variance of ocean temperatures. The roles of (epi)genetic variation, transgenerational and within-generation plasticity, and bet-hedging in adaptive potential were assessed. Exposure to directional warming (21°C) had detrimental effects on growth compared to ambient (17°C) conditions. Yet, when mothers were acclimated to 21°C, offspring reached larger sizes at 21°C as a result of transgenerational plasticity in response to predictable environmental cues of future environments, with optimised gene expression (transcriptomes) inherited from mothers underlying transgenerational benefits. However, when parents were acclimated to fluctuating environments (predictably variable or stochastic), mothers used bet-hedging strategies to cope with future environment uncertainty. In stochastically variable environments, offspring phenotypes were mostly influenced by within-generation plasticity and not transgenerational effects, and release of cryptic genetic variation for offspring size suggests hidden evolutionary potential to respond to changes in environmental predictability. Taken together, marine sticklebacks employ multiple adaptive strategies both within and across generations to cope with ocean warming and increasing climate variability.