Sperm and egg cells carry genetic and epigenetic information from parents to offspring, serving as a link between the past, present and future of a species. Unlike oocytes and somatic cells, which package their DNA with histones, the DNA of mature sperm is bound by protamines, highly basic and rapidly evolving proteins that are essential for the compaction of paternal chromatin. This differential packaging traces back >500 million years, yet its biological and evolutionary significance remains unknown. Protamines have thus far been considered passive structural elements that hyper condense and protect paternal DNA, however emerging biochemical, evolutionary, and developmental evidence calls for a need to revisit protamine proteins’ biological function. We have employed cutting-edge molecular, biochemical, and genetic approaches to investigate the role of protamines in fertility, early development, and evolution. Together, the findings presented here will increase our molecular understanding of these ancient, yet rapidly evolving proteins and may overturn the long-held dogma of their presumed function.