Declines in individuals' growth in exploited fish species are generally attributed to evolutionary consequences of size‐selective fishing or to plastic responses due to constraints set by changing environmental conditions dampening individuals' growth. However, other processes such as growth compensation and non‐directional selection can occur and their importance on the overall phenotypic response of exploited populations has largely been ignored. Using otolith growth data collected in European anchovy and sardine of the Bay of Biscay (18 cohorts from 2000 to 2018), we parameterized the breeder's equation to determine whether declines in size‐at‐age in these species were due to an adaptive response (i.e. related to directional or non‐directional selection differentials within parental cohorts) or a plastic response (i.e. related to changes in environmental). We found that growth at age‐0 in anchovy declined between parents and their offspring when biomass increased and the selective disappearance of large individuals was high in parents. Therefore, an adaptive response probably occurred in years with high fishing effort and the large increase in biomass after the collapse of this stock maintained this adaptive response subsequently. In sardine offspring, higher growth at age‐0 was associated with increasing biomass between parents and offspring, suggesting a plastic response to a bottom‐up process (i.e. a change in food quantity or quality). Parental cohorts in which selection favoured individuals with high growth compensation produced offspring high catch up growth rates, which may explain the smaller decline in growth in sardine relative to anchovy. Finally, on non‐directional selection differentials were not significantly related to the changes in growth at age‐0 and growth compensation at age‐1 in both species. Although anchovy and sardine have similar ecologies, the mechanisms underlying the declines in their growth are clearly different. The consequences of the exploitation of natural populations could be long lasting if density‐dependent processes follow adaptive changes.