The avian zoonotic agent for West Nile virus (WNV) can cause neuroinvasive disease in horses and humans and is expanding its range in Europe. Analyses of the risk for transmission to these hosts in non-endemic areas are necessary. Host preferences of mosquitoes (Diptera: Culicidae), the main vectors of WNV, were determined in Switzerland using animal-baited trap (horse, chickens) experiments at a natural and a periurban site. This was undertaken on four occasions during May–September 2014. In addition, the hosts of 505 blood-fed mosquitoes collected in a zoo and in the field were determined. Mosquito data obtained in the animal bait experiments were corrected for host weight and body surface area and by Kleiber's scaling factor. Collections of 11–14 different mosquito species were achieved with these approaches. Statistically significant host preferences were identified in three species in both approaches. The other species showed opportunistic feeding behaviours to varying extents. Specifically, the invasive species Hulecoeteomyia japonica (= Aedes japonicus) was identified for the first time as feeding on avians in nature. Abundance data, spatiotemporal activity and laboratory vector competence for WNV suggested that, in addition to the main WNV vector Culex pipiens, H. japonica and Aedimorphus vexans (= Aedes vexans) are the most likely candidate bridge vectors for WNV transmission in Switzerland.