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<i>Aedes aegypti</i>, the yellow fever mosquito, and <i>Aedes albopictus</i>, the Asian tiger mosquito, are the most significant vectors of dengue, Zika, and Chikungunya viruses globally. Studies examining host factors that control arbovirus transmission demonstrate that insect-specific viruses (ISVs) can modulate mosquitoes’ susceptibility to arbovirus infection in both in vivo and in vitro co-infection models. While research is ongoing to implicate individual ISVs as proviral or antiviral factors, we have a limited understanding of the composition and diversity of the <i>Aedes</i> virome. To address this gap, we used a meta-analysis approach to uncover virome diversity by analysing ~3000 available RNA sequencing libraries representing a worldwide geographic range for both mosquitoes. We identified ten novel viruses and previously characterised viruses, including mononegaviruses, orthomyxoviruses, negeviruses, and a novel bi-segmented negev-like group. Phylogenetic analysis suggests close relatedness to mosquito viruses implying likely insect host range except for one arbovirus, the multi-segmented Jingmen tick virus (<i>Flaviviridae</i>) in an Italian colony of <i>Ae. albopictus</i>. Individual mosquito transcriptomes revealed remarkable inter-host variation of ISVs within individuals from the same colony and heterogeneity between different laboratory strains. Additionally, we identified striking virus diversity in <i>Wolbachia</i> infected <i>Aedes</i> cell lines. This study expands our understanding of the virome of these important vectors. It provides a resource for further assessing the ecology, evolution, and interaction of ISVs with their mosquito hosts and the arboviruses they transmit.