Seminal extracellular vesicles (SEVs) carry a diverse array of bioactive molecules, including proteins, lipids, and nucleic acids, which influence sperm function and are implicated in modulating the female reproductive tract immune response after intromission. However, the full spectrum of SEV cargo involved in these processes remains incompletely defined. Here, we employed label-free quantitative high-resolution mass spectrometry to characterize the human SEV proteome, identifying 5,079 associated proteins. As the male reproductive tract origins of SEVs are still poorly understood, we first used the Human Protein Atlas Tissue Based Map of the Human Proteome to predict the male reproductive tract origin of the top 20 most abundant proteins. SEV proteins were thereby categorised as seminal vesicle-enriched (5/20 proteins), prostate-enriched (3/20 proteins), or no specific tissue enrichment (12/20 proteins) providing compelling evidence that in addition to the prostate, the seminal vesicles are a major contributor to the SEV pool. To explore the functions of SEV proteins, bioinformatic analysis using Ingenuity Pathway Analysis revealed enrichment in sperm- and immune-related functions, consistent with the predicted roles of SEV in events surrounding conception. Notably, we identified several proteins with established roles in sperm physiology and immune signalling that had not previously been postulated to be SEV signalling mediators. These included; Adenylate kinase isoenzyme (AK)2/9, calcium-binding tyrosine-phosphorylation regulated protein (CABYR), implicated in sperm motility, and immune regulators such as the toll-like receptor 4 ligand, high mobility group protein B1 (HMGB1), and the nuclear factor kappa-light-chain-enhancer of activated B cells (NFκB) inhibitor epsilon (NFκBIE). Interestingly, many other SEV proteins were associated with protein translation functions, potentially contributing to sperm survival and function in the female reproductive tract. Altogether, these findings expand the known SEV proteome and highlight proteins that may influence both male and female reproductive capacity.