Female mate choice is much more dynamic than we once thought. Mating decisions depend on both intrinsic and extrinsic factors, and these two may interact with one another. In this study, we investigate how responses to the social mating environment (extrinsic) change as individuals age (intrinsic). We first conducted a field survey to examine the extent of natural variation in mate availability in a population of threespine sticklebacks. We then manipulated the sex ratio in the laboratory to determine the impact of variation in mate availability on sexual signaling, competition, and mating decisions that are made throughout life. Field surveys revealed within season heterogeneity in mate availability across breeding sites, providing evidence for the variation necessary for the evolution of plastic preferences. In our laboratory study, males from both female-biased and male-biased treatments invested most in sexual signaling late in life, although they competed most early in life. Females became more responsive to courtship over time, and those experiencing female-biased, but not male-biased sex ratios, relaxed their mating decisions late in life. Our results suggest that social experience and age interact to affect sexual signaling and female mating decisions. Flexible behavior could mediate the potentially negative effects of environmental change on population viability, allowing reproductive success even when preferred mates are rare.