Abstract Phenotypic plasticity is essential for organisms to adapt to local ecological conditions. It is expected that mutualistic interactions, such as arbuscular mycorrhizal (AM) symbiosis, mediate plant phenotypic plasticity, although it is not clear to what extent this plasticity may be heritable (i.e. transgenerational plasticity). We tested for plant plasticity within‐ and across‐generations in response to AM symbiosis and varying water availability in a full factorial experiment over two generations, using a genetically uniform line of a perennial apomictic herb, Taraxacum brevicorniculatum. We examined changes in phenotype, performance and AM fungal colonization of the offspring throughout plant development. AM symbiosis and water availability triggered phenotypic changes during the life cycle of plants. Additionally, both factors triggered adaptive transgenerational effects especially detectable during the juvenile stage of the offspring. Water deficit and absence of AM fungi caused concordant plant phenotypic modifications towards a ‘stress‐coping phenotype’, both within and across generations. Parental environment also affected AM fungal colonization of the offspring. Juvenile offspring of amply watered parents and adut offspring of mycorrhizal parents had increasing length of root colonized by AM fungi when they were under water stress. Synthesis. We show that, in addition to providing beneficial transgenerational effects in offspring traits proxies of fitness (such as increased biomass, survival or nutritional status), AM symbiosis can trigger transgenerational plasticity in anatomical and physiological traits related to resource‐use acquisition, and further influence offspring AM fungal colonization. Our results show that AM symbiosis could improve plants' ability to cope with environmental stress, not only within, but also across generations.