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Abstract Global climate change is predicted to cause range shifts in the mosquito species that transmit pathogens to humans and wildlife. Recent modeling studies have sought to improve our understanding of the relationship between temperature and the transmission potential of mosquito‐borne pathogens. However, the role of the vertebrate host population, including the importance of host behavioral defenses on mosquito feeding success, remains poorly understood despite ample empirical evidence of its significance to pathogen transmission. Here, we derived thermal performance curves for mosquito and parasite traits and integrated them into two models of vector–host contact to investigate how vertebrate host traits and behaviors affect two key thermal properties of mosquito‐borne parasite transmission: the thermal optimum for transmission and the thermal niche of the parasite population. We parameterized these models for five mosquito‐borne parasite transmission systems, leading to two main conclusions. First, vertebrate host availability may induce a shift in the thermal optimum of transmission. When the tolerance of the vertebrate host to biting from mosquitoes is limited, the thermal optimum of transmission may be altered by as much as 5°C, a magnitude of applied significance. Second, thresholds for sustained transmission depend nonlinearly on both vertebrate host availability and temperature. At any temperature, sustained transmission is impossible when vertebrate hosts are extremely abundant because the probability of encountering an infected individual is negligible. But when host biting tolerance is limited, sustained transmission will also not occur at low host population densities. Furthermore, our model indicates that biting tolerance should interact with vertebrate host population density to adjust the parasite population thermal niche. Together, these results suggest that vertebrate host traits and behaviors play essential roles in the thermal properties of mosquito‐borne parasite transmission. Increasing our understanding of this relationship should lead us to improved predictions about shifting global patterns of mosquito‐borne disease.