Zika virus (ZIKV) is an orthoflavivirus primarily transmitted among humans by Aedes (Ae.) aegypti mosquitoes. Phylogenetically, ZIKV comprises two main lineages, referred to as the Asian and African lineages. Although all ZIKV outbreaks reported to date involved Asian lineage strains, experimental studies have shown that African lineage strains have a higher transmissibility in mosquitoes, indicating a significant epidemic potential. However, this has only been demonstrated in the globally invasive subspecies Ae. aegypti aegypti (Aaa), known to be more competent for ZIKV transmission than the native African subspecies. Whether African populations can efficiently transmit African ZIKV strains remains to be evaluated. Here, we used a combination of experimental and epidemiological modelling approaches to characterise the transmissibility and epidemic potential of two recent African ZIKV strains in several field-derived Ae. aegypti populations from West Africa. First, we confirmed that ZIKV susceptibility positively correlated with the proportion of Aaa genetic ancestry, regardless of the ZIKV strain involved. Next, we found that the transmission dynamics in mosquitoes depended on the specific combination of mosquito population and ZIKV strain. Finally, we implemented an agent-based model that integrates empirical data to quantify the epidemic potential of two distinct mosquito populations. Our epidemic simulations demonstrated significant differences in the potential for large outbreaks between the two populations. Together, these findings indicate that the risk of local ZIKV transmission in Africa varies significantly between mosquito populations, underscoring the importance of conducting localised assessments of Ae. aegypti genetic heterogeneity to effectively manage and mitigate the risk of outbreaks.