From invertebrate to vertebrate, females uptake sperm for a specific duration post-copulation known as the ejaculate holding period (EHP) before expelling un-stored sperm and the mating plug through sperm ejection. Our study uncovered that encountering males or mated females after mating substantially shortens EHP, a phenomenon we term ‘male-induced EHP shortening (MIES)’. MIES requires Or47b+ olfactory and ppk23+ gustatory neurons, activated by 2-methyltetracosane and 7-tricosene, respectively. These odorants raise cAMP levels in pC1b and c neurons, which are responsible for processing male courtship and regulating female receptivity. Elevated cAMP levels in pC1b and c reduce EHP and reinstate their responsiveness to male courtship cues, promoting re-mating with faster sperm ejection. This study establishes MIES as a genetically tractable model of sexual plasticity with a conserved neural mechanism.