Animal germ cells deploy a specialized small RNA-based silencing system, called the PIWI-interacting RNA (piRNA) pathway, to prevent aberrant expression of transposable elements and maintain genome integrity. In Drosophila germ cells, the majority of piRNA populations originate from dual-strand piRNA clusters, genomic regions highly enriched in transposon fragments, via an elaborate protein machinery centred on the heterochromatin protein 1 homolog, Rhino. Although Rhino binds to peptides carrying trimethylated H3K9 in vitro, it is not fully understood why it only occupies a fraction of H3K9me3-decorated heterochromatin in vivo. Recent work uncovered that Rhino is recruited to subsets of piRNA source loci by the zinc finger protein Kipferl. Here we identify a Kipferl-independent mode of Rhino targeting that is dependent on the histone H3 lysine 27 methyltransferase Enhancer of Zeste and the presence of H3K9me3 and H3K27me3 marks. Using a Kipferl-independent system, we find that Rhino, through a chromodomain dimer, specifically binds to loci marked by both H3K9me3 and H3K27me3. These results expand our understanding of the characteristic binding profile of the heterochromatin protein Rhino and reveal a role for dual histone modifications in defining the specificity of a chromatin binding protein.