The Balbiani body (Bb), a characteristic assembly of mitochondria and diverse organelles, occurs in oocytes of model species, including Drosophila melanogaster. Several functions that are critical for the proper development of oocytes and embryos have been attributed to Bb. Surprisingly, Bb has not been reported in oocytes of numerous insects, suggesting the potential absence of this structure in certain species. Here, we explore the distribution and fate of mitochondria during ovarian cyst development in the whirligig beetle, Gyrinus natator. In this species, oocytes do not contain Bb. However, a distinct assemblage of mitochondria and specific organelles, corresponding to Bb, forms in the germline cells of the ovarian cyst prior to the determination of the oocyte, indicating a novel mechanism of the Bb functioning. Fluorescent and ultrastructural analyses of the Gyrinus germline cells at different developmental stages also revealed that the behavior and fate of mitochondria are modulated by interactions with cisternae of the endoplasmic reticulum. We demonstrate that Gyrinus Bbs are involved in the selection and elimination of dysfunctional mitochondria and that these processes rely on mitochondrial networks and mitophagy. Furthermore, we found that a subset of mitochondria is associated with characteristic cellular structures termed sponge bodies. This association appears to facilitate the transport of the selected mitochondria to the germ plasm that forms within the posterior cytoplasm of the oocyte. Based on these results, a model for mitochondrial quality control and transfer within the ovarian cyst of G. natator is proposed.