Germline cysts are syncytia formed by incomplete cytokinesis of mitotic germline precursors (cystoblasts) in which the cystocytes are interconnected by cytoplasmic bridges, permitting the sharing of molecules and organelles. Among animals, such cysts are a nearly universal feature of spermatogenesis and are also often involved in oogenesis. Recent, elegant studies have demonstrated remarkable similarities in the oogenic cysts of mammals and insects, leading to proposals of widespread conservation of these features among animals. Unfortunately, such claims obscure the well-described diversity of female germline cysts in animals and ignore major taxa in which female germline cysts appear to be absent. In this review, I explore the phylogenetic patterns of oogenic cysts in the animal kingdom, with a focus on the hexapods as an informative example of a clade in which such cysts have been lost, regained, and modified in various ways. My aim is to build on the fascinating insights of recent comparative studies, by calling for a more nuanced view of evolutionary conservation. Female germline cysts in the Metazoa are an example of a phenomenon that-though essential for the continuance of many, diverse animal lineages-nevertheless exhibits intriguing patterns of evolutionary innovation, loss, and convergence.