The increased reproductive potential, size, shoot allocation, and growth rate of weedy plants may result from reduced resource allocation to other aspects of plant growth and defense. To investigate whether changes in resource allocation occurred during domestication or the evolution of weediness, we compared the mycorrhizal responsiveness, growth, and drought tolerance of nine native ruderal, nine agriculturally weedy (four U.S. weedy and five Australian weedy), and 14 domesticated populations (eight ancient landraces and six improved cultivars) of the common sunflower (Helianthus annuus). Domesticated sunflower cultivars were less drought tolerant, but had higher plant growth and fecundity and coarser roots than wild populations. There were no changes in level of drought tolerance between improved cultivars and ancient landrace plants, but there was an increase in allocation to flowers with recent selection. Weedy populations were intermediate between domesticated cultivars and native ruderal populations for plant growth rate, root architecture, and drought tolerance. Weedy populations benefited most from mycorrhizal inoculation by having fewer wilted leaves and wetter soil. Overall, we found that trade-offs between drought tolerance and several aspects of plant growth, including growth rate, allocation to flowering, and root architecture, govern evolution during sunflower domestication and the invasion of disturbed habitat.