Inheritance in mammals has traditionally been viewed as information encoded primarily in DNA sequence. Yet parental experiences can non-genetically shape the phenotypes of offspring, and even grand-offspring, through transgenerational epigenetic inheritance (TEI). While intergenerational inheritance to F1 progeny is well documented in rodents, TEI remains controversial, owing to a lack of robustly inherited phenotypes and incompletely defined mechanisms for transmitting information to and from the germline. Here, we provide evidence that the paternal immune system regulates epigenetic information in sperm to shape offspring phenotypes across generations. We find that T cell-deficient mice display defective sebum secretion and, strikingly, sire progeny and grand-progeny that share this defect despite having normal T cell numbers and function, establishing a robust, binary model of TEI. Sperm and epididymal small RNA profiles of T cell-deficient males differ markedly from wild-type males, particularly among RNAs transferred to sperm by epididymal extracellular vesicles (epididymosomes), implicating the epididymis in communicating paternal immune state to sperm. Complementing this chronic model, we show that acute paternal immune activation induces immune signaling within the male reproductive tract, rapidly remodels sperm small RNAs, and alters embryonic gene expression and development. Strikingly, offspring of immune-activated sires are protected from viral infection. Together, these findings reveal a soma-to-germline signaling axis through which paternal immune status is communicated to the male reproductive tract, encoded in sperm small RNAs, and transmitted at fertilization to program offspring development and immunity. Our work establishes the paternal immune system as a dynamic physiological regulator of epigenetic information in sperm and provides a new framework for understanding how paternal immune experiences shape the development, health, and disease susceptibility of future generations.