Developmental and adult thermal acclimation can have distinct, even opposite, effects on adult heat resistance in ectotherms. Yet, their relative contribution to heat-hardiness of ectotherms remains unclear despite the broad ecological implications thereof. Furthermore, the deterministic relationship between heat knockdown and recovery from heat stress is poorly understood but significant for establishing causal links between climate variability and population dynamics. Here, using Drosophila melanogaster in a full-factorial experimental design, we assessed the heat tolerance of flies in static stress assays, and document how developmental and adult acclimation interact with a distinct pattern to promote survival to heat stress in adults. We show that warmer adult acclimation is the initial factor enhancing survival to constant stressful high temperatures in flies, but also that the interaction between adult and developmental acclimation becomes gradually more important to ensure survival as the stress persists. This provides an important framework revealing the dynamic interplay between these two forms of acclimation that ultimately enhance thermal tolerance as a function of stress duration. Furthermore, by investigating recovery rates post-stress, we also show that the process of heat-hardening and recovery post-heat knockdown are likely to be based on set of (at least partially) divergent mechanisms. This could bear ecological significance as a trade-off may exist between increasing thermal tolerance and maximizing recovery rates post-stress, constraining population responses when exposed to variable and stressful climatic conditions.