Maternal effects of pathogen infection on progeny development and disease resistance may be adaptive and have important consequences for population dynamics. However, these effects are often context-dependent and examples of adaptive transgenerational responses from perennials are scarce, although they may be a particularly important mechanism generating variation in the offspring of long-lived species.Here, we studied the effect of maternal infection of Plantago lanceolata by Podosphaera plantaginis, a fungal parasite, on the growth, flower production and resistance of the progeny of six maternal genotypes in nutrient-rich and nutrient-poor environments. For this purpose, we combined a common garden study with automated phenotyping measurements of early life stages, and an inoculation experiment.Our results show that the effects of infection on the mother plants transcend to impact their progeny. Although maternal infection decreased total leaf and flower production of the progeny by the end of the growing season, it accelerated early growth and enhanced resistance to the pathogen P. plantaginis.We also discovered that the effects of maternal infection affected progeny development and resistance through a three way-interaction between maternal genotype, maternal infection status and nutrient availability. Synthesis. Our results emphasize the importance of maternal effects mediated through genotypic and environmental factors in long-living perennials and suggest that maternal infection can create a layer of phenotypic diversity in resistance. These results may have important implications for both epidemiological and evolutionary dynamics of host-parasite interactions in the wild.