Vertebrate reservoirs of arboviruses are often infected with microfilariae (MF). Laboratory studies have shown that MF can enhance the infectivity of arboviruses to mosquitoes. Soon after being ingested, MF penetrate the mosquito midgut. If the host blood also contains virus (i.e., vertebrate is dually infected), penetrating MF may introduce virus into the hemocoel. This can transform otherwise virus-incompetent mosquito species into virus-competent species and simultaneously accelerate viral development, allowing mosquitoes to transmit virus sooner than normal. This phenomenon is termed microfilarial enhancement of arboviral transmission. The prevalence of MF is very high in many passerine populations in North America. Therefore, we investigated if microfilarial enhancement could have facilitated the establishment and rapid spread of West Nile virus (WNV) across the mid-western United States. Our investigations revealed that mosquitoes, WNV, and passerine MF do interact in nature because; 1) 17% of 54 common grackles (Quiscalus quiscula L.), 8% of 26 American robins (Turdus migratorius L.), and 33% of three eastern kingbirds (Tyrannus tyrannus L.) were concurrently microfilaremic and seropositive to WNV; 2) feeding activities of mosquitoes overlapped temporally with the appearance of MF in the blood of common grackles; 3) mosquitoes fed on common grackles and American robins in nature; and 4) mosquito ingestion of two taxonomically distant species of passerine MF (i.e., Chandlerella quiscali and Eufilaria spp.) resulted in penetration of mosquito midguts. To estimate the theoretical effect that MF enhancement could have on WNV transmission in areas of high MF prevalence, vectorial capacity values were calculated for Culex mosquitoes feeding on common grackles, whereby MF enhancement was either invoked or ignored. For Cx. pipiens, vectorial capacity increased over three-fold when potential effects of MF were included in the calculations. For Cx. tarsalis, the effect was less (i.e., 1.4-fold increase). Closer attention should be paid to the potential of MF to enhance mosquito transmission of arboviruses.