The PIWI-interacting RNA (piRNA) pathway is crucial for maintaining genomic integrity by suppressing transposable elements in animal germlines. Despite this recognized germline function, piRNAs are widely expressed in somatic tissues across arthropod species, raising questions about somatic functions of the piRNA pathway. Here, we studied the Aedes albopictus mosquito, which expresses four out of its seven PIWI genes in both germline and somatic tissues. We generated Piwi6 knockout Ae. albopictus cell lines, and observed a substantial upregulation of Long Terminal Repeat (LTR)-retrotransposons. Prominent among these is an element that seems to encode intact gap, pol and env genes, which we named Aedes endogenous retrovirus 1 (AeERV1). Our findings indicate that Piwi6 transcriptionally silences AeERV1 by depositing repressive H3K9me3 histone marks, leading to heterochromatin formation. Intriguingly, Piwi6 gene knockdown in adult Ae. albopictus mosquitoes resulted in AeERV1 upregulation in both somatic and germline tissues. Our data indicate that piRNAs mediate transcriptional transposon silencing in the mosquito soma and suggest that this function may be evolutionarily conserved across arthropod species.