Transgenerational plasticity (TGP) occurs when offspring exhibit plasticity in traits induced by the environments experienced by their parents, and represents a non-genetic mechanism of inheritance. Evidence that traits can be transmitted to future generations by means other than genetic inheritance has caused a surge of interest in epigenetic inheritance, but evidence for epigenetic modifications being both adaptive and heritable remains scarce. What features would make a species most prone to evolve a system of epigenetically-mediated adaptive TGP? Here we use population-genetic models modified to include epigenetic induction and inheritance to investigate if and when epigenetically-mediated adaptive TGP would be expected to evolve for a population subdivided between two habitats connected by migration. We show that differences in the direction of selection between the two habitats drives the evolution of epigenetically-mediated adaptive TGP. With low migration, the strength of indirect selection in favour of epigenetically-mediated adaptive TGP increases with migration rate. Yet, with higher migration, the opposite trend is observed. We predict that species subdivided between habitats that differ in the direction of selection with moderate migration rates between the habitats would be most likely to evolve epigenetically-mediated adaptive TGP if costs of producing such systems are not too high.