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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 <i>Aedes</i> <i>aegypti</i> and <i>Ae. albopictus</i> from Brazil and two of <i>Ae.</i> <i>aegypti</i> and one of <i>Culex quinquefasciatus</i> 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. <i>Cx. quinquefasciatus</i> was refractory to infection with all virus strains. In contrast, although competence varied with geographical origin, Brazilian and New Caledonian <i>Ae. aegypti</i> could transmit the three ZIKV lineages, with a strong advantage for the African lineage (the only one reaching saliva one-week after challenge). Brazilian <i>Ae. albopictus</i> populations were less competent than <i>Ae. aegypti</i> populations. <i>Ae. albopictus</i> generally exhibited almost no transmission for Asian and American lineages, but was efficient 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.