The Eastern treehole mosquito, Aedes triseriatus (Say), is the primary vector of La Crosse virus (LACV) in the United States. LACV is maintained in natural populations in part by transovarial transmission from infected females to their progeny. Our understanding of the innate immune response in mosquito ovaries is a fundamental step toward understanding the transmission cycle of LACV and other vertically transmitted arthropod-borne viruses. We investigated signaling mechanisms between the nutrient content of the vertebrate blood meal and activation of mosquito egg development. In particular, the target of rapamycin (TOR) serine/threonine protein kinase is a central regulator of nutritional signaling, and we examined the roles of TOR and its downstream target, S6K, in Ae. triseriatus by RNA interference. We also examined the transcriptomes of Ae. triseriatus and Ae. aegypti (L.) ovaries by Illumina RNA-seq. We assembled 17,743 novel transcript sequences from Ae. triseriatus ovary mRNA using a novel and highly accurate assembly method, and we identified genes that are differentially regulated during the processes of follicular atresia, apoptosis, and autophagy. Distinct differences exist between the transcriptional regulation of Ae. triseriatus and Ae. aegypti oogenesis. TOR and many other proteins with previously unknown function are transcriptionally regulated during apoptosis and autophagy in mosquito ovaries during oogenesis.