The semi-aquatic bugs (Heteroptera, Gerromorpha) conquered water surfaces worldwide and diversified to occupy puddles, ponds, streams, lakes, mangroves, and even oceans. Critical to this life style is the evolution of sets of hairs that allow these insects to maintain their body weight on the water surface and protect the animals against wetting and drowning. In addition, the legs of these insects are equipped with various grooming combs that are important for cleaning and tidying the hair layers for optimal functional efficiency. Here we show that the hairs covering the legs of water striders represent innervated bristles. Genomic and transcriptomic analyses revealed that in water striders the achaete-scute complex, known to control bristle development in flies, contains only the achaete-scute homologue (ASH) gene due to the loss of the gene asense. Using RNA interference, we show that ASH plays a pivotal role in the development of both bristles and grooming combs in water striders. Our data suggest that the ASH locus may have contributed to the adaptation to water surface lifestyle through shaping the hydrophobic bristles that prevent water striders from wetting and allow them to exploit water surface tension.