This study describes the coevolution of sperm length and female spermatheca size in the backswimmer Notonecta glauca. The species exhibits exceptionally long sperm, characterized by an unusually elongated acrosome, a short nucleus, and a long flagellum featuring a conventional 9 + 9+2 microtubular axoneme and two large mitochondrial derivatives. The spermatheca is equally elongated, comprising a spiralized proximal tract with a unique and novel ultrastructure, a long middle cuticular duct, and a terminal bulb. The spiralized region is lined by an epithelium covered with an extraordinarily thick cuticle composed of orthogonal pillars that terminate in pointed apices. In mated females, a thick secretion layer accumulates between the cuticle and the epithelium, which is enriched with mitochondrial complexes. A comparative analysis of virgin and mated females suggests that the epithelium in mated females actively reabsorbs fluid from the duct lumen. The cuticular duct, a simple and elongated tract, has its lumen compartmentalized by cuticular projections. The terminal bulb, in turn, features an epithelium made up of secretory cells with an extracellular cistern for secretion storage and duct-forming cells rich in longitudinal microtubules. These cells are equipped with ducts that transport the stored secretion to the lumen. Overall, the findings confirm that the size of the female spermatheca influences sperm morphology, underscoring a tight coevolution between these traits.