Two alternative hypotheses may account for the low fruit:flower ratios regularly observed in many species of plants. First, a low fruit:flower ratio may be a passive “nonadaptive” consequence of external stressors that destroy flowers or limit their pollination. Alternatively, a low fruit:flower ratio may be a result of adaptations that enhance plant fitness, perhaps by allowing the plants to compensate for the very stressors that limit fruit set. We tested these nonadaptive and adaptive hypotheses using Solanum carolinense (horsenettle), an herbaceous plant that generally exhibits a low fruit:flower ratio. Horsenettle often suffers substantial flower loss to herbivores and fruit set can be pollen limited. We present experimental evidence that neither floral destruction by herbivores nor pollen limitation directly affected fruit:flower ratio. Instead, the low fruit:flower ratio was an adaptive consequence of the production of “surplus” flowers. These flowers served as reserve ovaries that enabled the plants to compensate fully for both floral herbivory and incomplete pollination.