Significance Aging-associated diseases are increasingly common in an aging global population. However, the contributors and origins of differential risk for unhealthy aging remain poorly understood. Using a mouse model, we found that offspring of aged fathers exhibited a reduced life span and more pronounced aging-associated pathologies than animals sired by young fathers. Tissue of offspring and aged fathers revealed shared epigenetic signatures and showed altered activation states of longevity-related cell signaling. Our results suggest that variability in aging trajectories could derive, in part, from the age at conception of the father, a possibility that warrants human epidemiological investigation.