The northern fowl mite, Ornithonyssus sylviarum, is the most damaging ectoparasite on egg-laying hens in the United States. One potential strategy for management is breeding for mite resistance. Genes of white leghorn chickens linked to the major histocompatibility complex (MHC) were previously identified as conferring more (B21 haplotype) or less (B15 haplotype) mite resistance. However, immune responses can be energetically costly to the host and affect the economic damage incurred from mite infestations. We tested energy costs (resting metabolic rate) of mite infestations on egg-laying birds of both MHC B-haplotypes. Resting metabolic rates were documented before (pre-) mite infestation, during (mid-) infestation, and after peak (late) mite infestation. Mite scores, economic parameters (egg production, feed consumption), and physiological aspects such as skin inflammation and skin temperature were recorded weekly. Across experiments and different infestation time points, resting metabolic rates generally were not affected by mite infestation or haplotype, although there were instances of lower metabolic rates in infested versus control hens. Skin temperatures were recorded both at the site of mite feeding damage (vent) and under the wing (no mites), which possibly would reflect a systemic fever response. Ambient temperatures modified skin surface temperature, which generally was not affected by mites or haplotype. Feed conversion efficiency was significantly worse (4.9 to 17.0% depending on trial) in birds infested with mites. Overall egg production and average egg weight were not affected significantly, although there was a trend toward reduced egg production (2 to 8%) by infested hens. The MHC haplotype significantly affected vent skin inflammation. Birds with the mite-resistant B21 haplotype showed earlier onset of inflammation, but a reduced overall area of inflammation compared to mite-susceptible B15 birds. No significant differences in resting energy expenditure related to mite infestation or immune responses were detected. Potential breeding for resistance to mite infestation using these two haplotypes appears to be neutral in terms of impact on hen energy costs or production efficiency, and may be an attractive option for future mite control.