It is generally assumed that the reproductive success of both males and females is not limited by the availability of ejaculates. However, when male ejaculate production is physiologically constrained, the maintenance of high fertility can be an important determinant of fitness. Under the phenotype-linked fertility hypothesis, females can maximise their fertility by choosing mates on the basis of external phenotypic indicators (exaggerated sexual ornaments or displays) of male reproductive quality. I test the phenotype-linked fertility hypothesis in the stalk-eyed fly Cyrtodiopsis dalmanni, a species characterised by sexual dimorphism in the length of the eyestalks that project laterally from the head (eyespan). I demonstrate that females prefer large eyespan males as mates and exhibit higher fertility when housed with large eyespan males than when housed with small eyespan males. I also show that male eyespan predicts the growth rates and final sizes of the accessory glands and testes of males raised under different levels of nutritional stress. Thus male eyespan is a reliable indicator of male reproductive quality, and female preference for this trait can directly increase female fitness through fertility assurance. The higher fertility of large eyespan males is associated with the ability to copulate at a higher frequency rather than greater success on a per-mating basis. Using artificial selection experiments and behavioural observations, I provide evidence that male mating frequency is physiologically constrained by the size of the accessory glands. As eyespan reflects male accessory gland size, females can improve their chances of obtaining an ejaculate by choosing mates with large eyespan. Moreover, I show that males allocate larger ejaculates to females that offer a greater number of fertilisation opportunities. Based on my results, I have proposed a physiological mechanism for the signalling of male mating frequency by male eyespan mediated by circulating levels of juvenile hormone.