Germ cell specification is an essential step in sexually reproducing animals. Echinoderms possess diverse representatives of the main mechanisms that result in this cell fate determination. Sea urchins use an inherited mechanism, whereas sea stars rely on the ancestral, induced mechanism. Blimp1 (B lymphocyte-induced maturation protein-1) is a transcriptional regulator reported in mice to function in the induction of germline cells. Here, we identify the dynamic function of Blimp1 during development in a comparative approach using the purple sea urchin, Strongylocentrotus purpuratus (inherited germline) and the batstar, Patiria miniata (induced germline). We found that Blimp1 is important for germ cell specification in both species and that multiple Blimp1 isoforms result from differential mRNA splicing in each animal. Each isoform of Blimp1 functions in distinct expression of germline determinants, including Vasa and Nanos. These results show that Blimp1 is a conserved and key regulator for germ cell specification, but divergent in function as a result of post-transcriptional modification. Overall, we conclude that Blimp1 is an intersectional node in diverse germline specification strategies and supports the concept that differential mRNA splicing is an essential mechanism in germ cell formation.