The genital chamber is a structure that is important for mating, egg progression, and fertilization in female crickets. The activity and efferent control of the genital chamber and its retractor, muscle 2, are characterized using electrophysiology, intracellular dye injections, and immunohistochemistry in a dissected preparation of female Acheta domesticus. Rhythmic activity in nerves 7v and 8v underlies movements of the genital chamber, and rhythmically-active motor neurons in the terminal abdominal ganglion supply the genital chamber and muscle 2. Some of these motor neurons were identified on the basis of intracellularly-recorded activity, axonal projections, target muscle, and/or central anatomy. Rhythmic 8v motor neurons in the terminal abdominal ganglion have two morphological types; one type shows diffuse or stringy projections and the physiological characteristic of soma spikes. Rhythmic motor neurons do not show properties such as plateau potentials, which are consistent with endogenous oscillation; it is suggested that they receive rhythmic synaptic drive. A bilateral pair of identified rhythmic motor neurons in the 8th segment contains serotonin and projects to the genital chamber. Serotonergic fibers on the genital chamber are the endings of this pair of neurons exclusively. Other serotonergic neurons in the terminal ganglion project to motor and integrative areas, and serotonin is differentially localized in sensory projection areas of the 7th and 8th versus the 9th and 10th neuromeres. These results suggest that serotonin could be involved in the modulation of mechanosensory information, as well as modulating pattern-generating circuitry in the terminal ganglion. This system presents a model for investigating the role of serotonin in neuromuscular transmission, and in the integration of neural circuits for behavior.