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Simple Summary: Aedes aegypti and Ae. albopictus mosquitoes are competent transmitters of Zika virus (ZIKV) and are widely distributed throughout the state of Florida. Investigations of the long-term maintenance of the virus that allows outbreaks to persist in adverse environmental conditions are limited. One mechanism for arboviral maintenance in nature is vertical transmission (VT) of a virus passed directly from parent to offspring during reproduction. This study assesses the potential of Florida Ae. aegypti and Ae. albopictus to vertically transmit ZIKV. To address this gap in our understanding of this critical risk parameter, we orally exposed Florida F3 generation Ae. aegypti and Ae. albopictus to ZIKV infected blood meals using a dose of ZIKV within the range of viremia levels experienced by infected humans. We observed low VT in both Ae. aegypti (1.1–3.2%) and Ae. albopictus (0–0.3%) mosquitoes; despite imbibing infected blood at titers that yielded high susceptibility to infection and modest horizontal transmission rates. Filial infection rates; testing individual mosquitoes; for Ae. aegypti and Ae. albopictus were 6–10% and 0–6.4%, respectively. Both invasive Stegomyia mosquitoes were capable of vertically transmitting ZIKV under laboratory conditions; and approximately 5% of female progeny of Ae. aegypti were capable of transmitting ZIKV upon first bite. The Zika virus pandemic of 2015, with mosquitoes Aedes aegypti and Ae. albopictus as the putative vectors, prompted public health concerns and the need to improve our understanding of both the horizontal and vertical transmission of Zika virus. Local transmission is especially concerning for Florida, where these two mosquito species are abundant and widespread throughout much of the year. Here, we evaluate the relative vertical transmission and filial infection rate of progeny of Florida Ae. aegypti and Ae. albopictus following ingestion of infected blood by parental mosquitoes at either 6 or 7 log10 plaque forming units/mL of Zika virus. Florida Ae. aegypti exhibited higher rates of disseminated infection than Ae. albopictus, consistent with other studies indicating greater permissibility of Zika virus in Ae. aegypti. We observed low vertical transmission in both Ae. aegypti (1.1–3.2%) and Ae. albopictus (0–0.3%) mosquitoes, despite imbibing infected blood at titers that yielded high susceptibility to infection and modest horizontal transmission rates. Filial infection rates, testing individual mosquitoes for Ae. aegypti and Ae. albopictus, were 6–10% and 0–6.4%, respectively. Both these invasive Stegomyia mosquitoes were capable of vertically transmitting Zika virus under laboratory conditions, and approximately 5% of female progeny of Ae. aegypti were capable of transmitting Zika virus upon first bite. [ABSTRACT FROM AUTHOR]