The mother sporocyst is the least understood digenean life cycle stage. This study provides the first detailed description of the neuromusculature and reproductive apparatus of mother sporocysts in the hemiuroid digenean Bunocotyle progenetica, a monoxenous parasite of White Sea mud snails, using transmission electron microscopy and fluorescent staining for muscles, FMRFamide-related peptides (FaRP), and serotonin (5HT). These parthenitae lack a germinal mass and have only a few germinal elements, which explains their limited reproductive potential. Germinal cells are incorporated into the syncytial brood-cavity lining, asynchronously maturing and forming germinal balls, which develop into rediae within the cavity. Rediae are expelled through a birth canal differentiated into three regions; their expulsion involves coordinated action of circular sphincter muscles and several extrinsic muscles. Sporocysts are highly mobile, with a dense subtegumental network of circular and longitudinal muscles. Subtegumental myocyte reconstruction showed that each perikaryon is linked to several myofibrils. The nervous system, although lacking distinct ganglia, is well-differentiated, with numerous neurons and at least three types of tegumental sensilla. FaRP-immunoreactive (IR) somata surround the birth canal, forming a nerve net around its middle region and two posterior longitudinal nerves. The unusually abundant 5HT-IR neurons are distributed throughout the body, but most lie in the posterior region. 5HT-IR cells form an anterior nerve ring, from which several nerves project anteriorly and two main nerves extend posteriorly, along with additional nerves. The morphology of the studied sporocysts is discussed in the context of current knowledge on the parthenital biology and development in B. progenetica.