Transgenerational plasticity in plants is an increasingly recognized phenomenon, yet it is mostly unclear whether transgenerational plasticity is relevant to both the fitness of the plant and its interacting species. Using monoclonal strains of the giant duckweed ( Spirodela polyrhiza) and its native herbivore, the waterlily aphid ( Rhopalosiphum nymphaeae), we assessed whether pre-treating plants with copper excess, both indoors and outdoors, induces transgenerational plasticity in plant defences that alter plant and herbivore fitness. Outdoors, copper pre-treatment tended to increase plant growth rates under recurring copper excess. Indoors, copper pre-treatment either increased or decreased plant growth rates under recurring conditions, depending on the plant genotype. Copper pre-treatment induced anthocyanins that protected plants against copper toxicity, and these elevated levels were transgenerationally retained. Copper pre-treatment also transgenerationally increased the levels of 12-oxo-phytodienoic acid (OPDA), a jasmonate precursor. Nevertheless, aphids grew up to 50% better when the plants were pre-treated with copper. The increased aphid growth was likely caused by transgenerationally elevated OPDA levels, as aphids grew better when jasmonates were externally applied to plants. Taken together, this study shows that transgenerational plasticity is relevant to both plant and herbivore fitness, which highlights the role of transgenerational plasticity in plant evolution and species interactions.