Phenotypic plasticity has the potential to influence environmental adaptation on extremely short evolutionary timescales. Transgenerational plasticity allows parents to provision their offspring for rapid environmental shifts in as little as one generation. We hypothesized that transgenerational plasticity is used by multivoltine organisms to maximize fitness under predictable seasonal fluctuations in environmental conditions. This study examined how seasonal thermal variation (i.e., average temperature and acute heat stress), impacts physiological tolerance, maternal provisioning, and developmental plasticity across multiple generations of the direct-developing bivoltine eelgrass sea hare, Phyllaplysia taylori. Seasonally-acclimatized adults from successive generations were acclimated at 13, 17 and 21°C to assess thermal tolerance limits and plasticity, and the effects of thermal acclimation and heat stress on reproductive output in one generation were assessed to characterize transgenerational plasticity. There was an interactive effect of seasonal generation and acclimation temperature on heat tolerance limits. Total maternal investment in egg laying decreased by 39% under at warmer average temperatures and declined by 78% with the addition of acute heat stress. Acute heat stress reduced hatching success by an average of 8%. Transgenerational plasticity maintained total viable offspring under two seasonal conditions regularly experienced in the wild, despite different offspring density in egg masses within these conditions and large individual differences in offspring output. We find that existing transgenerational plasticity on average cannot maintain current offspring numbers (as reflected in the 13°C and 17°C acclimation conditions) under warmer conditions (21°C), and is thus inadequate to compensate for the effects of climate change.