Soma-germline interactions control fertility at many levels, including stem cell proliferation, meiosis and gametogenesis, yet the nature of these fundamental signaling mechanisms and their potential evolutionary conservation are incompletely understood. In C. elegans, a sperm-sensing mechanism regulates oocyte meiotic maturation and ovulation, tightly coordinating sperm availability and fertilization. Sperm release the major sperm protein (MSP) signal to trigger meiotic resumption (meiotic maturation) and to promote contraction of the follicle-like gonadal sheath cells that surround oocytes. Using genetic mosaic analysis, we show that all known MSP-dependent meiotic maturation events in the germline require Galpha(s)-adenylate cyclase signaling in the gonadal sheath cells. We show that the MSP hormone promotes the sustained actomyosin-dependent cytoplasmic streaming that drives oocyte growth. Furthermore, we demonstrate that efficient oocyte production and cytoplasmic streaming require Galpha(s)-adenylate cyclase signaling in the gonadal sheath cells, thereby providing a somatic mechanism that coordinates oocyte growth and meiotic maturation with sperm availability. We present genetic evidence that MSP and Galpha(s)-adenylate cyclase signaling regulate oocyte growth and meiotic maturation in part by antagonizing gap-junctional communication between sheath cells and oocytes. In the absence of MSP or Galpha(s)-adenylate cyclase signaling, MSP binding sites are enriched and appear clustered on sheath cells. We discuss these results in the context of a model in which the sheath cells function as the major initial sensor of MSP, potentially via multiple classes of G-protein-coupled receptors. Our findings highlight a remarkable similarity between the regulation of meiotic resumption by soma-germline interactions in C. elegans and mammals.