Abstract: In mosquitoes, hearing is driven by sound-induced mechanical displacement of the flagellum which stimulates the auditory efferent systems in the Johnston's organs (JO) situated at the base of their antenna. Male mosquitoes rely on sound for close-range communication during mating, while frog-biting female mosquitoes from specific species use hearing to detect distant frog mating calls for host identification. Our study focuses on the auditory system of Uranotaenia lowii, a mosquito species that specializes in feeding exclusively on frogs by eavesdropping on their mating calls. Using an integrative approach, we examined how directional sound localization occurs in these mosquitoes through biomechanical, electrophysiological, neuroanatomical, and behavioral investigations of their ears. We used Laser Doppler Vibrometry to examine the mechanical vibrations of their antennae in response to sound, electrophysiology to measure neural responses, immunohistochemistry to map the auditory innervation of the JO, and phonotaxis experiments to study their behavioral attraction to acoustic cues. Our research goes further by hypothesizing that the acoustic preferences of Ur. lowii are shaped by evolutionary pressures to maximize reproductive success. We tested this by evaluating how different frog species—native, sympatric, allopatric, and invasive—affect mosquito phonotaxis and offspring production. Our findings illuminate the auditory adaptations that facilitate host detection in Ur. lowii, revealing how these mosquitoes fine-tune their sensory systems to thrive in their unique ecological niche. This study significantly broadens our understanding of mosquito biology and contributes to a deeper understanding of mosquito acoustic communication, particularly in the specialized context of host-parasite interactions.