Mosquitoes use multiple host-associated cues to efficiently locate sources of blood. While detection mechanisms for longer-range cues like CO2 and odors have been widely studied, less is known about how mosquitoes sense the short-range heat and humidity gradients surrounding hosts. We recently demonstrated that heat-seeking in the malaria vector Anopheles gambiae is driven by cooling-activated neurons requiring the Ionotropic Receptor (IR) subunit IR21a. Although heat is a powerful short-range mosquito attractant, genetic disruption of heat seeking alone only modestly impacts overall host detection, suggesting other cues act in parallel with heat near hosts. We now show that An. gambiae and the arbovirus vector Aedes aegypti both require another IR, IR93a, to maintain host attraction and feed efficiently on warmed blood. By genetically targeting IR93a, we identify the mosquito humidity-sensing (hygrosensory) system, and show that IR93a is required for hygrosensation and thermosensation (in IR21a+ neurons). These systems function in parallel to drive host proximity detection. After blood feeding, gravid females also require IR93a to seek water for egg-laying. These data show that two major vectors of human disease use similar mechanisms to locate hosts and oviposition sites and demonstrate the overall importance of short-range cue detection for complex mosquito behaviors.