In many species, male secondary sexual traits have evolved via female choice as they confer indirect (i.e. genetic) benefits or direct benefits such as enhanced fertility or survival. In humans, the role of men's characteristically masculine androgen-dependent facial traits in determining men's attractiveness has presented an enduring paradox in studies of human mate preferences. Male-typical facial features such as a pronounced brow ridge and a more robust jawline may signal underlying health, whereas beards may signal men's age and masculine social dominance. However, masculine faces are judged as more attractive for short-term relationships over less masculine faces, whereas beards are judged as more attractive than clean-shaven faces for long-term relationships. Why such divergent effects occur between preferences for two sexually dimorphic traits remains unresolved. In this study, we used computer graphic manipulation to morph male faces varying in facial hair from clean-shaven, light stubble, heavy stubble and full beards to appear more (+25% and +50%) or less (−25% and −50%) masculine. Women (N = 8520) were assigned to treatments wherein they rated these stimuli for physical attractiveness in general, for a short-term liaison or a long-term relationship. Results showed a significant interaction between beardedness and masculinity on attractiveness ratings. Masculinized and, to an even greater extent, feminized faces were less attractive than unmanipulated faces when all were clean-shaven, and stubble and beards dampened the polarizing effects of extreme masculinity and femininity. Relationship context also had effects on ratings, with facial hair enhancing long-term, and not short-term, attractiveness. Effects of facial masculinization appear to have been due to small differences in the relative attractiveness of each masculinity level under the three treatment conditions and not to any change in the order of their attractiveness. Our findings suggest that beardedness may be attractive when judging long-term relationships as a signal of intrasexual formidability and the potential to provide direct benefits to females. More generally, our results hint at a divergence of signalling function, which may result in a subtle trade-off in women's preferences, for two highly sexually dimorphic androgen-dependent facial traits.