Abstract Recent evidence suggests that stressed plants employ epigenetic mechanisms to transmit acquired resistance to their progeny. However, little is known about the evolutionary and ecological significance of this transgenerational acquired resistance (TAR). In this study, we have used a full factorial design to study the specificity, costs and stability of TAR following exposure of Arabidopsis thaliana to increasing stress intensities by a biotrophic pathogen, a necrotrophic pathogen, and soil salinity. All stresses incrementally reduced parental growth, while salt stress additionally impacted reproductive success. Biotrophic and necrotrophic pathogens, but not salt, increased resistance of progeny against the stress experienced by their parents (i.e., in matched environments). In mis-matched environments, however, pathogen-elicited TAR was associated with costs from increased susceptibility to other stresses. Furthermore, the stability of pathogen-elicited TAR over one stress-free generation and its associated costs were proportional to parental disease severity, suggesting that plants use stress intensity as an environmental proxy to adjust TAR investment. We conclude that pathogen-elicited TAR is an adaptive and deterministic parental effect that is associated with ecological costs. Accordingly, our study provides evolutionary and ecological context to the epigenetic TAR response. Key words: Adaptive parental effects; Arabidopsis; Phenotypic plasticity; Plant stress; Transgenerational acquired resistance.