The female reproductive system of the free-living nematode family Cephalobidae is examined by means of differential interference contrast, scanning electron and fluorescent microscopy. The model nematode Caenorhabditis elegans and the predatory nematode Prionchulus punctatus are also included in this study; the former mainly to test our results with the very detailed knowledge of this model organism, the latter to provide a representative of the more distantly related Enoplea. In this comparative approach, the analysed gonad structures are discussed with respect to their functional and phylogenetic significance. The general cellular composition of the cephalobid gonad – namely an oviduct comprising two rows of four cells, a distinctly offset spermatheca consisting of 8-16 cells, and a uterus composed of distinct cell rows – differs from all known Nematoda except that of the plant-parasitic Tylenchomorpha. Despite the striking evolutionary conservation of the cellular architecture of the cephalobid gonad there is a complex subcellular specialisation, namely a significant and functionally relevant variation in myofilament organisation, both among Cephalobidae and between major groups of nematodes. We demonstrate the presence of microfilaments that vary in pattern among species and that may play an important role in egg propulsion. The phenomenon of endotokia matricida, in which eggs do not leave the female body, is found to be associated with a massive rupture of the cytoskeleton in the uterus wall. The complexity of the myofibril structure and the associated potential to propagate oocytes actively cannot be solely explained by differences in phylogenetic history, but is also linked to body diameter. In the larger Acrobeloides maximus, the proximal end of the ovary sheath is adorned with 12 distinct longitudinal bands, antibody binding positively for paramyosin, while in the smaller Cephalobus cubaensis myofilament organisation is at random.