Despite their conserved functional role in sexually reproducing organisms, spermatozoa are a diverse and rapidly evolving cell type. This phenomenon is largely attributed to sexual selection in polygamous species where sperm from multiple males compete to fertilize a limited number of oocytes. Drosophila have proven to be a particularly informative model system for the study of spermatogenesis and in this review we discuss how the characterization of the Drosophila melanogaster sperm proteome has advanced our understanding of the evolutionary genomics of sperm form and function. We summarize the molecular evolutionary characteristics of sperm genes and highlight recent evidence demonstrating the importance of novel gene creation in the evolution of sperm function and competitive ability. Comparative proteomic evidence is also provided, supporting an overall functional conservation between the Drosophila and mouse sperm proteomes. This analysis reveals a diverse repertoire of proteins functioning in proteolytic pathways, as well as the presence of proteins of the complement and innate immunity systems. We propose that these pathways may have functional relevance to post-mating female immunological responses as well as coevolved interactions with pathways expressed in the female reproductive tract, including those involved in sperm-oocyte recognition and fertilization.