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Given the rising risk of extreme weather caused by climate change, enhancement of abiotic stress resistance in crops is increasingly urgent. But will the development of stress-resistant cultivars come at the cost of yield under ideal conditions? We hypothesize that this need not be inevitable, because resistance alleles with minimal pleiotropic costs may evade artificial selection and be retained in crop germplasm. Genome-wide association (GWA) analyses for variation in plant performance and flooding response were conducted in cultivated sunflower, a globally important oilseed. We observed broad variation in flooding responses among genotypes. Flooding resistance was not strongly correlated with performance in control conditions, suggesting no inherent trade-offs. Consistent with this finding, we identified a subset of loci conferring flooding resistance, but lacking antagonistic effects on growth. Genetic diversity loss at candidate genes underlying these loci was significantly less than for other resistance genes during cultivated sunflower evolution. Despite bottlenecks associated with domestication and improvement, low-cost resistance alleles remain within the cultivated sunflower gene pool. Thus, development of cultivars that are both flooding-tolerant and highly productive should be straightforward. Results further indicate that estimates of pleiotropic costs from GWA analyses explain, in part, patterns of diversity loss in crop genomes.