Seminal fluid proteins (SFPs) exert potent effects on male and female fitness. These rapidly evolving and molecularly diverse proteins derive from multiple male secretory cells and tissues. In Drosophila melanogaster most SFPs are produced in the accessory glands, which are composed of ~1000 fertility-enhancing ‘main cells’ and ~40, more functionally cryptic, ‘secondary cells’. Previous work shows that inhibition of BMP-signalling in secondary cells suppresses secretion, leading to a surprising uncoupling of normal female post-mating responses: refractoriness stimulation is impaired, but offspring production is not. Secondary cell secretions might therefore make a highly specific contribution to the seminal proteome and ejaculate function; alternatively, they might play a more global – but hitherto-undiscovered – role in regulating SFPs and their interconnected functions. Here, we present data that supports the latter model. We show that in addition to previously reported phenotypes, secondary cell-specific BMP-inhibition compromises sperm storage and increases female sperm use efficiency. Moreover, it alters sperm competition: second male sperm enter storage more slowly, ejaculates are ejected later, and first male paternity share improves. This result suggests a novel constraint on ejaculate evolution whereby female refractoriness and sperm competitiveness cannot be simultaneously maximised. Using quantitative proteomics, we reveal changes to the seminal proteome that surprisingly encompass alterations to main cell-derived proteins, indicating important cross-talk between classes of SFP-secreting cells. Our results demonstrate that ejaculate composition and function emerge from the integrated action of multiple secretory cell-types suggesting that modification to the cellular make-up of seminal fluid-producing tissues is an important factor in ejaculate evolution.