Homeostasis of adult tissues is maintained by a small number of stem cells, which are sustained by their niches. In the female germline stem cell (GSC) niche, Decapentaplegic (Dpp) is the primary factor that promotes GSC self-renewal. However, the mechanism regulating expression in the niche is largely unknown. Here, we identify a 2.0 kb fragment located in a 5' -regulatory region of the locus containing enhancer activity that drives its expression in the niche. This region is distinct from a previously characterized 3' -regulatory enhancer responsible for expression in imaginal discs. Our data demonstrate that Engrailed, a homeodomain-containing transcription factor that serves as a cap cell marker, binds to this region and regulates expression in cap cells. Further data suggest that En forms a complex with Nejire (Nej), the ortholog of histone acetyltransferase CBP/p300, and directs Nej to this -regulatory region where Nej functions as the co-activator for expression. Therefore, our study defines the molecular pathway controlling expression in the ovarian stem cell niche.