Uncontrolled transposable element (TE) insertions and excisions can cause chromosome breaks and mutations with dramatic deleterious effects. The PIWI interacting RNA (piRNA) pathway functions as an adaptive TE silencing system during germline development. Several essential piRNA pathway proteins appear to be rapidly evolving, suggesting that TEs and the silencing machinery may be engaged in a classical “evolutionary arms race.” Using a variety of molecular evolutionary and population genetic approaches, we find that the piRNA pathway genes rhino, krimper, and aubergine show patterns suggestive of extensive recurrent positive selection across Drosophila species. We speculate that selection on these proteins reflects crucial roles in silencing unfamiliar elements during vertical and horizontal transmission of TEs into naïve populations and species, respectively.