The bag of marbles (bam) gene plays a critical role in early gametogenesis in Drosophila melanogaster, where it promotes germline stem cell (GSC) daughter differentiation through interaction with benign gonial cell neoplasm (bgcn). Despite its essential role in D. melanogaster, comparative analyses across Drosophila species reveal functional divergence. In particular, bam is not essential for GSC differentiation in D. teissieri, raising questions about the evolutionary history and flexibility of this function. Using AlphaFold2 and AlphaFold Multimer, we compared predicted protein structures of Bam and the Bam:Bgcn complex across four species (D. melanogaster, D. simulans, D. yakuba, and D. teissieri). Despite notable amino acid sequence divergence, high-confidence structural regions remain conserved, suggesting that changes in Bam protein structure are unlikely to explain its functional divergence in D. teissieri. This supports the hypothesis that Bam may not be integrated into the essential GSC differentiation pathway in D. teissieri, rather than having lost function due major structural changes.To explore the evolutionary origins of bam's function, we generated bam null alleles in a more distantly related species, D. americana. The essential role of bam in GSC differentiation is conserved in D. americana, indicating that this function predates the melanogaster species group and may be more basal to the Drosophila genus. Expanding this analysis, we surveyed 366 genes known to regulate GSC differentiation in D. melanogaster across 15 other Drosophila species and two outgroups. Approximately 8% of these genes are absent in at least one species, providing strong evidence for developmental systems drift (DSD) in gametogenesis. These findings support a model in which core developmental processes are conserved, but the specific genetic components can vary across evolutionary time. Patterns of amino acid diversification and positive selection in bam are consistent with the Selection, Pleiotropy, and Compensation (SPC) model, suggesting adaptive changes, possibly involving interactions with endosymbiotic Wolbachia, followed by compensatory evolution to maintain protein structure and broader developmental function.