encodes one of the two fly CPEB proteins. These widely conserved proteins bind to the 3'UTRs of target messenger RNAs (mRNAs) and activate or repress their translation. We show here that a positive autoregulatory loop driven by the gene propels the specification of oocyte identity in egg chambers. Oocyte fate specification is mediated by a 3'UTR-dependent mechanism that concentrates mRNAs and proteins in one of the two pro-oocytes in the 16-cell germline cyst. When the 3'UTR is deleted, mRNA and protein fail to localize and all 16 cells become nurse cells. In wild type, the oocyte is specified when and other gene products concentrate in a single cell in region 2b of the germarium. A partially functional 3'UTR replacement delays oocyte specification until the egg chambers reach stage 2 of oogenesis. Before this point, mRNA and protein are unlocalized, as are other markers of oocyte identity, and the oocyte is not specified. After stage 2, ∼50% of the chambers successfully localize in a single cell, and this cell assumes oocyte identity. In the remaining chambers, the autoregulatory loop is not activated and no oocyte is formed. Finally, maintenance of oocyte identity requires continuous activity.