Acute environmental stressors such as short-term exposure to pollutants can have lasting effects on organisms, potentially impacting future generations. Parental exposure to toxicants can result in changes to the epigenome (e.g., DNA methylation) that are passed down to subsequent, unexposed generations. However, it is difficult to gauge the cumulative population-scale impacts of epigenetic effects from laboratory experiments alone. Here, we developed a size- and age-structured delay-coordinate population model to evaluate the long-term consequences of epigenetic modifications on population sustainability. The model emulated changes in growth, mortality, and fecundity in the F0, F1, and F2 generations observed in experiments in which larval Menidia beryllina were exposed to environmentally relevant concentrations of bifenthrin (Bif), ethinylestradiol (EE2), levonorgestrel (LV), or trenbolone (TB) in the parent generation (F0) and reared in clean water up to the F2 generation. Our analysis suggests potentially dramatic population-level effects of repeated, chronic exposures of early-life stage fish that are not captured by models not accounting for those effects. Simulated exposures led to substantial declines in population abundance (LV and Bif) or near-extinction (EE2 and TB) with the exact trajectory and timeline of population decline dependent on the combination of F0, F1, and F2 effects produced by each compound. Even acute one-time exposures of each compound led to declines and recovery over multiple years due to lagged epigenetic effects. These results demonstrate the potential for environmentally relevant concentrations of commonly used compounds to impact the population dynamics and sustainability of an ecologically relevant species and model organism.