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Oocytes must be exceptionally large cells in order to support embryonic development. Throughout animal phylogeny, a specialized cell called a syncytium, wherein many nuclei share a continuous cytoplasm, achieves oogenesis. The syncytial nature of germline architecture is key to its function and depends on conserved components of the cortical cytoskeleton. Septins form non‐polar cytoskeletal polymers that associate with membranes. In the syncytial germline of the nematodeCaenorhabditis elegans, septins are highly enriched on the cortex and generally required for fertility, but the role of septins in the germline is poorly understood. We report that theC. elegansseptins, UNC‐59 and UNC‐61, are important for germline extension during development, the maintenance of its syncytial architecture, and production of oocytes. While much of our findings substantiate the idea that the twoC. elegansseptins act together, we also found evidence that they have distinct functions. Loss of UNC‐61 perturbed germline extension during germline development, while the loss of UNC‐59 function severely affected germline architecture in adult hermaphrodites. Consultation of clustering results from a large‐scale high‐throughput screen suggested that septins are involved in germ cell proliferation and/or differentiation. In sum, our findings implicate a conserved cytoskeletal component in the complex architecture of a germline syncytium.