Regulated secretion typically involves the trafficking of specific secretory products into dense-core granule (DCG) compartments, which mature and are then released by exocytosis after stimulation. These compartments must subsequently be rapidly replenished to retain secretory capacity. However, the mechanisms involved are largely unexplored. We have studied this problem in fixed and live secondary cells (SCs) of the Drosophila accessory gland (AG), which contain huge secretory compartments (> 5 µm diameter), thus providing a unique system to study DCG biogenesis and secretion. Here we demonstrate that each SC contains approximately ten large DCGs loaded with the Bone Morphogenetic Protein (BMP) Decapentaplegic (Dpp). When flies mate, roughly four DCG compartments are rapidly released from SCs, and autocrine BMP signalling, as measured by nuclear pMad staining, is immediately increased. Two of the secreted compartments are restored within 6 hours and by 24 hours, complete replenishment is achieved. The release of secretory compartments is dependent on their maturity, limiting the secretion of additional DCGs during rapid multiple matings. Interestingly, the replenishment of DCGs is regulated by BMP signalling, which is also required for secretion of these compartments, potentially through its effects on DCG maturation. Our study therefore highlights a central function for Dpp in matching biogenesis of new DCGs to elevated release of these compartments from SCs after mating. Notably, BMP signalling is crucial for secretion in other cell types, including insulin-secreting pancreatic beta cells and Drosophila motor neurons. Our new model potentially reflects a more general role for BMPs in providing a read-out for DCG release that ensures DCG numbers are maintained following regulated secretion.