Zika virus (ZIKV) has caused severe epidemics in South America beginning in 2015, following its spread through the Pacific. We comparatively assessed the vector competence of ten populations of Aedes aegypti and Ae. albopictus from Brazil and two of Ae. aegypti and one of Culex quinquefasciatus from New Caledonia to transmit three ZIKV isolates belonging to African, Asian and American lineages. Recently colonized mosquitoes from eight distinct sites from both countries were orally challenged with the same viral load (107 TCID50/mL) and examined after 7, 14 and 21 days. Cx. quinquefasciatus was refractory to infection with all virus strains. In contrast, although competence varied with geographical origin, Brazilian and New Caledonian Ae. aegypti could transmit the three ZIKV lineages, with a strong advantage for the African lineage (the only one reaching saliva one-week after challenge). Brazilian Ae. albopictus populations were less competent than Ae. aegypti populations. Ae. albopictus generally exhibited almost no transmission for Asian and American lineages, but was e cient in transmitting the African ZIKV. Viral surveillance and mosquito control measures must be strengthened to avoid the spread of new ZIKV lineages and minimize the transmission of viruses currently circulating.