Genetic inheritance underpins evolutionary theories of aging, but the role that nongenetic inheritance plays is unclear. Parental age reduces the life span of offspring in a diverse array of taxa but has not been explained from an evolutionary perspective. We quantified the effect that maternal age had on the growth and maturation decisions, life history, rates of senescence, and life span of offspring from three Daphnia pulex clones collected from different populations. We then used those data to test general hypotheses proposed to explain maternal age effects on offspring life span. Three generations of breeding from young or old mothers produced dramatic differences in the life histories of fourth-generation offspring, including significant reductions in life span. The magnitude of the effect differed between clones, which suggests that genetic and nongenetic factors ultimately underpin trait inheritance and shape patterns of aging. Older parents did not transmit a senescent state to their offspring. Instead, offspring from older ancestors had increased early-life reproductive effort, which resulted in an earlier onset of reproductive senescence, and an increased rate of actuarial senescence, which shortened their life span. Our results provide a clear example of the need to consider multiple inheritance mechanisms when studying trait evolution.