Transgenerational plasticity, the influence of the environment experienced by parents on the phenotype and fitness of subsequent generations, is being increasingly recognized. Human-altered environments, such as those resulting from the increasing use of pesticides, may be major drivers of such cross-generational influences, which in turn may have profound evolutionary and ecological repercussions. Most of these consequences are, however, unknown. Whether transgenerational plasticity elicited by pesticide exposure is common, and the consequences of its potential carryover effects on fitness and population dynamics, remains to be determined. Here, we investigate whether exposure of parents to a common pesticide elicits intra-, inter-, and transgenerational responses (in F0, F1, and F2 generations) in life history (fecundity, longevity, and lifetime reproductive success), in an insect model system, the seed beetle Callosobruchus maculatus. We also assessed sex specificity of the effects. We found sex-specific and hormetic intergenerational and transgenerational effects on longevity and lifetime reproductive success, manifested both in the form of maternal and paternal effects. In addition, the transgenerational effects via mothers detected in this study are consistent with a new concept: terminal investment transgenerational effects. Such effects could underlie cross-generational responses to environmental perturbation. Our results indicate that pesticide exposure leads to unanticipated effects on population dynamics and have far-reaching ecological and evolutionary implications.