Although non-genetic inheritance is thought to play an important role in plant ecology and evolution, evidence for adaptive transgenerational responses is scarce. Here, we investigated the consequences of copper excess on offspring defense and fitness in the duckweed Spirodela polyrhiza across multiple generations. We found that descendants of large monoclonal populations (>10,000 individuals) that grew for 30 generations under copper excess exhibited negative fitness during the first few generations and positive fitness in consecutive generations under recurring stress. Similarly, propagating individual plants for 5 or 10 generations under copper excess decreased plant fitness when 5 generations and improved fitness when 10 generations passed between initial and recurring stress. Fitness benefits under recurring stress were partially associated with avoidance of excessive copper but not increased flavonoid accumulation. Taken together, these data demonstrate time-dependent adaptive transgenerational responses under recurring stress, which highlights the importance of non-genetic inheritance for plant ecology and evolution.