Integrating long-term ecological observations with experimental findings on species response and tolerance to environmental stress supports an understanding of climate effects on population dynamics. Here, we combine the two approaches, laboratory experiments and analysis of multi-decadal time-series, to understand the consequences of climate anomalies and ongoing change for the population dynamics of a eurythermal littoral species, Carcinus aestuarii. For the generation of cause and effect hypotheses we investigated the thermal response of crab embryos at four developmental stages. We first measured metabolic rate variations in embryos following acute warming (16–24 °C) and after incubation at 20 and 24 °C for limited periods. All experiments consistently revealed differential thermal responses depending on the developmental stage. Temperature-induced changes in metabolic activity of early embryonic stages of blastula and gastrula suggested the onset of abnormal development. In contrast, later developmental stages, characterized by tissue and organ differentiation, were marginally affected by temperature anomalies, indicating enhanced resilience to thermal stress. Then, we extended these findings to a larger, population scale, by analyzing a time-series of C. aestuarii landings in the Venice lagoon from 1945 to 2010 (ripe crabs were recorded separately) in relation to temperature. Landings and extreme climatic events showed marked long-term and short-term variations. We found negative relationships between landings and thermal stress indices on both timescales, with time lags consistent with an impact on crab early life stages. When quantitatively evaluating the influence of thermal stress on population dynamics, we found that it has a comparable effect to that of the biomass of spawners. This work provides strong evidence that physiological responses to climatic anomalies translate into population-level changes and that apparently tolerant species may be impacted before the ontogeny of eurythermy. These ontogenetic bottlenecks markedly shape population dynamics and require study to assess the effects of global change.