Updated publication reference for PubMed record(s): 28847004. Nuclear small RNA pathways safeguard genome integrity by establishing transcription-repressing heterochromatin at transposable elements. This inevitably also targets the transposon-rich source loci of the small RNAs themselves. How small RNA source loci are efficiently transcribed while transposon promoters are potently silenced, is not understood. Here, we show that transcription of Drosophila piRNA clusters—small RNA source loci in animal gonads—is enforced through RNA Polymerase II pre-initiation complex formation within repressive heterochromatin. This is accomplished through the TFIIA-L paralog Moonshiner, which is recruited to piRNA clusters via the Heterochromatin Protein-1 variant Rhino. Moonshiner triggers transcription initiation within piRNA clusters by recruiting the TATA box-binding protein (TBP)-related factor TRF2, an animal TFIID core variant. Thus, transcription of heterochromatic small RNA source loci relies on direct recruitment of the core transcriptional machinery to DNA via histone marks rather than sequence motifs, a concept that we argue is a recurring theme in evolution.