Species showing color polymorphisms—the presence of two or more genetically determined color morphs within a single population—are excellent systems for studying the selective forces driving the maintenance of genetic diversity. Despite a shortage of empirical evidence, it is often suggested that negative frequency-dependent mate preference by males (or diet choice by predators) results in fitness benefits for the rare female morph (or prey type). Moreover, most studies have focused on the male (or predator) behavior in these systems and largely overlooked the importance of female (or prey) resistance behavior. Here, we provide the first explicit test of the role of frequency-dependent and frequency-independent intersexual interactions in female polymorphic damselflies. We identify the stage of the mating sequence when frequency-dependent selection is likely to act by comparing indexes of male mate preference when the female has little (females presented on sticks), moderate (females in cages), and high (females free to fly in the field) ability to avoid male mating attempts. Frequency-dependent male preferences were found only in those experiments where females had little ability to resist male harassment, indicating that premating interactions most likely drive negative frequency-dependent selection in this system. In addition, by separating frequency-dependent male mating preference from the baseline frequency-independent component, we reconcile the seemingly contradictory results of previous studies and highlight the roles of both forms of selection in maintaining the polymorphism at a given equilibrium. We conclude that considering interactions among all players—here, males and females—is crucial to fully understanding the mechanisms underlying the maintenance of genetic polymorphisms in the wild.