SummaryCompetition is a key factor affecting the performance and co‐existence of species. Most ecological research on competition treats species’ populations as phenotypically homogenous. However, plant populations typically contain genetic variation for multiple traits and have the potential to rapidly adapt to changing environments.Recent theoretical and empirical research suggests that such variation and evolution may affect the ecological outcome of competitive interactions. We conducted a series of experiments to test the hypothesis whether genetic variation for competitive traits in a native plant (Oenothera biennis) affects the performance and diversity of competing plant species.In greenhouse and field experiments, the presence ofO. biennisreduced the performance and diversity of neighbouring plant species.In greenhouse experiments, we detected heritable variation inO. biennisfor above‐ground and below‐ground growth, andO. biennisvaried genetically in response to competition, indicating the potential for adaptive evolution in response to selection by competitors.Variation amongO. biennisgenotypes also affected the performance of neighbouring plants in the greenhouse, whereby genetic variation inO. biennisshoot : root ratio explained up to 41% of the variation in the performance of an exotic grass (Bromus inermis).Despite effects ofO. biennisgenotype onB. inermisin the greenhouse, variable soil fertility had a much stronger effect on the grass's performance, and there were no effects ofO. biennisgenotype on neighbouring plants in the field.Synthesis. Our results show that interspecific competition affected the biomass and diversity of plants, but heritable variation in competitive ability ofO. biennisis not expected to affect short‐term ecological dynamics in this system. Nevertheless,O. biennishas the potential to influence co‐existence over longer timescales by adapting to competitors.