There appear to be few reports in the literature regarding the host-poultry red mite (Dermanyssus gallinae) immunological relationship, despite the negative impact D. gallinae can have on both bird welfare and egg production, as well as its potential to act as a reservoir of zoonotic infections. The current study investigated the effect of either continuous infestation (CI) for 22 days or repeated infestation (RI) for four 24-h periods 7 days apart with D. gallinae on humoral immunity (IgM and IgY) and Th1/Th2 cytokine mRNA expression in peripheral blood mononuclear cells (PBMC) compared to non-infested controls. Serum IgY levels and IgM concentration were significantly higher in CI than RI and control birds although Th1 and Th2 mRNA expression in PBMC did not differ significantly between groups. D. gallinae appeared to modify reproductive behaviour and progeny survival following successive feeding events. In the RI group, the proportion of eggs/mite was significantly higher (P <0.05) after first infestation than later infestations while larval/nymphal mortality was significantly higher (P <0.05) after the first two infestations than later infestations. These data suggest that D. gallinae might adopt a feeding strategy of minimal host interference while D. gallinae could determine host immune status via nymphal/larval survival rates. Further research is required to better understand the host immunomodulation or avoidance strategy of D. gallinae as well as whether the mite is able to determine host immunocompetence perhaps using progeny survival.