Long non-coding RNAs (lncRNAs) play critical regulatory roles in various cellular and metabolic processes in mosquitoes and all other organisms studied thus far. In particular, their involvement in essential processes such as reproduction makes them potential targets for the development of novel pest control approaches. However, their function in mosquito biology remains largely unexplored. To elucidate the role of lncRNAs in mosquitoes’ reproduction and vector competence for arboviruses, we have implemented a computational and experimental pipeline to mine, screen, and characterize lncRNAs related to these two biological processes. Through analysis of publicly available Zika virus (ZIKV) infection-regulatedAedes aegyptitranscriptomes, at least six lncRNAs were identified as being significantly upregulated in response to infection in various mosquito tissues. The roles of these ZIKV-regulated lncRNAs (designatedZinc1,Zinc2,Zinc3,Zinc9,Zinc10andZinc22), were further investigated by dsRNA-mediated silencing studies. Our results show that silencing ofZinc1,Zinc2, andZinc22renders mosquitoes significantly less permissive to ZIKV infection, while silencing ofZinc22also reduces fecundity, indicating a potential role forZinc22in trade-offs between vector competence and reproduction. We also found that silencing ofZinc9significantly increases fecundity but has no effect on ZIKV infection, suggesting thatZinc9may be a negative regulator of oviposition. Our work demonstrates that some lncRNAs play host factor roles by facilitating viral infection in mosquitoes. We also show that lncRNAs can influence both mosquito reproduction and permissiveness to virus infection, two biological systems with important roles in mosquito vectorial capacity.