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Ecological and medical researchers are investing great effort to determine the role of Maternally‐Derived Stress (MDS) as an inducer of phenotypic plasticity in offspring. Many researchers have interpreted phenotypic responses as unavoidable negative outcomes (e.g., small birth weight, high anxiety); however, a biased underestimate of the adaptive potential of MDS‐induced effects is possible if they are not viewed within an ecologically relevant or a life‐history optimization framework. We review the ecological and environmental drivers of MDS, how MDS signals are transferred to offspring, and what responses MDS induces. Results from four free‐living vertebrate systems reveals that although MDS induces seemingly negative investment trade‐offs in offspring, these phenotypic adjustments can be adaptive if they better match the offspring to future environments; however, responses can prove maladaptive if …