The molecular mechanisms by which environmental cues influence reproductive success are not well understood. In this study, we identify a genomic cluster of serpentine receptor B (SRB) chemosensory receptors that modulate sperm motility performance within the hermaphrodite reproductive tract. SRB chemoreceptors signal via GOA-1 and EGL-30 G protein pathways in male ciliated amphid sensory neurons, including ASI and ASK. SRB signaling is both necessary and sufficient in amphids to modulate sperm motility performance. The neuropeptide ligands FLP-21 and FLP-18, and their receptor NPR-1, act together with SRB chemoreceptors to transduce signals to the testis. We show that SRB signaling promotes metabolic and cytoskeletal gene expression during spermatogenesis. Changes in sperm mitochondrial respiratory chain complex subunit mRNA levels affect sperm velocity and reversal frequency, impairing their ability to respond to guidance cues called prostaglandins. These results show that chemosensation has a profound impact on sperm function, with each sex manipulating sperm performance to optimize their individual reproductive success. Current efforts aim to better understand the sensory cues that control SRB pathways and evolution of the SRB circuits.