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We performed an arboviral survey in mosquitoes from four endemic Ecuadorian cities (Huaquillas, Machala, Portovelo and Zaruma) during the epidemic period 2016–2018. Collections were performed during the pre-rainy season (2016), peak transmission season (2017) and post-rainy season (2018). Ae. aegypti mosquitoes were pooled by date, location and sex. Pools were screened by RT-PCR for the presence of ZIKV RNA, and infection rates (IRs) per 1,000 specimens were calculated. A total of 2,592 pools (comprising 6,197 mosquitoes) were screened. Our results reveal high IRs in all cities and periods sampled. Overall IRs among female mosquitoes were highest in Machala (89.2), followed by Portovelo (66.4), Zaruma (47.4) and Huaquillas (41.9). Among male mosquitoes, overall IRs were highest in Machala (35.6), followed by Portovelo (33.1), Huaquillas (31.9) and Zaruma (27.9), suggesting that alternative transmission routes (vertical/venereal) can play important roles for ZIKV maintenance in the vector population of these areas. Additionally, we propose that the stabilization of ZIKV vertical transmission in the vector population could help explain the presence of high IRs in field-caught mosquitoes during inter-epidemic periods. Author summary: Zika virus (ZIKV) is a mosquito-borne virus native to Africa that can cause a wide range of symptoms in humans, including neurological complications and fetal abnormalities. ZIKV arrived to South America in 2015, and quickly spread through the continent. In Ecuador, this virus caused several thousand infections during 2016 and 2017, but its incidence dropped suddenly thereafter, with just 11 cases reported between 2018 and 2022. The reasons behind this abrupt decrease are not well understood. In this work, we performed an arboviral survey in mosquitoes from four endemic Ecuadorian cities during the period 2016–2018. We screened 2,592 pools (comprising 6,197 specimens) for the presence of ZIKV, and estimated infection rates in female and male mosquitoes. We found high infection rates in all cities and periods sampled. Considering the low incidence of human cases during 2018, our results suggest that in our study areas the virus could be maintained by mechanisms that either do not depend on human infection, or cause low rates of symptomatic infections. High rates of ZIKV infection in male mosquitoes found during our study suggest that vertical and/or venereal transmission routes could play important roles in the inter-epidemic maintenance of this pathogen in our study area. [ABSTRACT FROM AUTHOR]