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West Nile virus (WNV) is maintained cryptically primarily in avian (passerine) populations, where it is transmitted by Culex spp. mosquitoes. Mosquito-control measures currently include physical activities to reduce mosquito-breeding sites and the application of mosquito larvicides or aerosolized insecticides to kill adults (adulticides) when arboviral diseases such as WNV or Zika virus are detected in mosquito populations. Organochlorine, organophosphorus, carbamate, and pyrethroid insecticides are often used. Previous work suggests an effect of pyrethroids on the immune system in a variety of vertebrates. We examined the effects of exposure to aerosolized Permanone (R) 30:30 insecticide (permethrin and piperonyl butoxide in soy oil vehicle) at approximately 10(3) to 10(6) times potential environmental concentrations on the response of captive zebra finches (Taeniopygia guttata) to experimental challenge with WNV. Compared to vehicle control birds, WNV outcome was unchanged (65% of birds produced a viremia) in the low exposure (9.52 +/- 3.13mg/m(3) standard deviation [SD] permethrin) group but reduced in the high exposure (mean 376.5 +/- 27.9mg/m(3) SD permethrin) group (30% were viremic; p<0.05). After clearing WNV infection, birds treated with Permanone regained less body mass than vehicle-treated birds (p<0.001). The present study suggests that exposure to aerosolized Permanone insecticide at levels exceeding typical application rates has the potential to not change or to mildly enhance a bird's resistance to WNV. Environ Toxicol Chem 2017;36:3376-3386. Published 2017 Wiley Periodicals Inc. on behalf of SETAC. This article is a US government work and, as such, is in the public domain in the United States of America.