Sperm development is accompanied by post-testicular modification of sperm as they transit the epididymis- a process necessary for fertilization competency. However, unlike well-studied mammalian systems, less is known about what, if any, similar sperm modifications occur in in other taxonomic groups, including Drosophila. However, recent work on the Dmel sperm proteome (DmSP, ~1100 proteins) revealed that ~50% of genes encoding the DmSP were not significantly expressed in the testis suggesting they were inserted following spermatogenesis. RNA-seq analysis confirmed that these genes were significantly expressed in the terminal epithelium and seminal vesicle (further termed “TE/SV” tissue). This raised the intriguing possibility that these proteins are inserted into sperm after exit from the testis. Analysis of the seminal vesicle proteome revealed functional enrichment in protein secretion, translocation and targeting similar to those found in secretory cells and polarized epithelia of the mammalian epididymis suggesting a similar function in the TE/SV. To further explore tissue-specific origin of the DmSP we identified a subset of genes not overexpressed in the testis (FA "down") but present in significant protein levels (determined by spectral counting). From this list, three readily available CPTI protein-trap lines of the DmSP were identified and their cell- and tissue-specific expression patterns were monitored by epifluorescence microscopy. As predicted, all three proteins showed low level testis expression and high expression in the seminal vesicle and the terminal epithelium suggesting that sperm exiting the testis were modified during transit into, or residence within, the TE/SV. Taken together these results suggest that Drosophila sperm are extensively modified following exit from the testis during transit into, and storage within, the seminal vesicle in a manner akin to that observed in the mammalian epididymis. As such, an “insect epididymis” could provide a rich new experimental model system useful for the study of fertility and related reproductive processes in both arthropods and vertebrates.