Male sea lamprey (Petromyzon marinus) release a multi-component sex pheromone that attracts females and elicits courtship behaviors. Previous research indicates the male pheromone mimics a nonsexual larval cue, but that females discriminate between the larval cue and male pheromone — which each consist, in part, of the attractant 3kPZS — using the larval compound PZS as a behavioral antagonist of 3kPZS. Although PZS is the more abundant component in the larval cue and 3kPZS the more abundant component in the male pheromone, males produce high physiological concentrations of PZS as a precursor to 3kPZS and release small quantities of PZS into the water. To test the hypothesis that male variation in PZS release guides female mate choice, we 1) characterized male variation in release of 3kPZS and PZS and 2) determined whether females can discriminate among males’ pheromone signals using variation in PZS release. Wild males sampled off spawning nests released 3kPZS and PZS at ratios ranging from 1.5:1 to 263:1 (3kPZS: PZS; n = 77). Repeated sampling from the onset of sexual maturation until death, which occurs naturally at the end of lamprey’s single spawning season, revealed that males gradually released more PZS. In an in-stream behavioral assay, females preferred mixtures of 3kPZS and PZS at ratios typical of recently matured males (90:1) over males nearer to death (30:1). Sperm analyses indicated that males with the most preferred 3kPZS: PZS ratio had lower quality sperm than less preferred males. We postulate that avoidance of PZS arose as a mechanism to prevent orientation towards larvae, but incidentally biases female choice away from males closer to senescence.