Cytoplasmic polyadenylation is a key mechanism of gene control. In Caenorhabditis elegans, GLD-2 and GLD-3 provide the catalytic and RNA-binding subunits, respectively, of a major cytoplasmic poly(A) polymerase (PAP). Here, we identify RNP-8 as a second GLD-2 partner. RNP-8 binds GLD-2 and stimulates GLD-2 activity to form a functional PAP, much like GLD-3. Moreover, GLD-2/RNP-8 and GLD-2/GLD-3 exist as separate complexes that form selectively during development, and RNP-8 and GLD-3 appear to have distinct RNA-binding specificities. Therefore, GLD-2 can form either of two discrete PAPs. In C. elegans hermaphrodites, gamete production begins with spermatogenesis and transitions later to oogenesis. We suggest that the combinatorial use of GLD-2 contributes to this transition, as GLD-2/GLD-3 promotes spermatogenesis, whereas GLD-2/RNP-8 specifies oogenesis. Indeed, RNP-8 and GLD-3 antagonize each other, as evidenced by genetic cosuppression and molecular competition for GLD-2 binding. We conclude that GLD-2 and its binding partners control gamete identity.