Climate warming not only enhances the activity of ticks but may also promote the activation and proliferation of pathogens within them, thereby increasing the risk of tick-borne disease transmission. Defensins, as key effector molecules of tick innate immunity, effectively regulate the levels of pathogens in the host; however, the cooperative mechanisms between defensins and other immune molecules remain unclear. This study investigated the impact of elevated temperature on the proliferation of Rickettsia within the hard tick Haemaphysalis longicornis. By employing RNA interference to silence specific defensin genes and combining quantitative proteomic analysis, we found that following defensin knockdown, the load of Rickettsia in ticks increased to some extent, while the expression of several immune-related proteins, including Hemolectin and serine protease inhibitors, was significantly upregulated. These results suggest that ticks may activate a compensatory immune regulatory network to cope with the loss of key defense molecules. This study systematically reveals the elastic regulatory mechanisms of the tick immune network under infection pressure and provides a new perspective for a deeper understanding of the “host–pathogen–environment” interaction.