Non-native plants are now a pervasive feature of ecosystems across the globe1. One hypothesis for this pattern is that introduced species occupy open niches in recipient communities2,3. If true, then non-native plants should often benefit from low competition for limiting resources that define niches. Many plants have evolved larger size after introduction, consistent with increased access to limiting resources4–9. It has been difficult to test whether larger size reflects adaptation to exploit open resources, however, because vacant niches are generally challenging to identify in plants. Here we take advantage of a situation in which a highly invasive non-native plant, Centaurea solstitialis L. (yellow starthistle, hereafter ‘YST’), occupies a well-described environmental niche, wherein water is a known limiting resource10,11. We use a glasshouse common environment and climatic niche modeling to reveal that invading YST has evolved a higher-fitness life history at the expense of increased dependence on water. Critically, historical declines in resident competitors have made water more available for introduced plants11,12, demonstrating how native biodiversity declines can open niches and create opportunities for introduced species to evolve increased resource use, a potentially widespread basis for introduction success and the evolution of invasive life histories.