The expected strong directional selection for traits that increase a male's mating ability conflicts with the frequent observation that within species, males may show extreme variation in sexual traits. These male reproductive polymorphisms are usually attributed to direct male-male competition. It is currently unclear, however, how directional selection for sexually selected traits may convert into disruptive selection, and if female preference for elaborate traits may be an alternative mechanism driving the evolution of male polymorphism. Here we explore this mechanism using the polyandric dwarf spider Oedothorax gibbosus as a model. We first show that males characterized by conspicuous cephalic structures serving as a nuptial feeding device (‘gibbosus males’) significantly outperform other males in siring offspring of previously fertilized females. However, significant costs in terms of development time of gibbosus males open a mating niche for an alternative male type lacking expensive secondary sexual traits. These ‘tuberosus males’ obtain virtually all fertilizations early in the breeding season. Individual-based simulations demonstrate a hitherto unknown general principle, by which males selected for high investment to attract females suffer constrained mating opportunities. This creates a vacant mating niche of unmated females for non-investing males and, consequently, disruptive selection on male secondary sexual traits.