Epigenetic inheritance, the transmission of phenotypic traits across generations without changes to the DNA sequence, provides a mechanism by which parental environmental and physiological influences shape offspring development and health. Here we investigate the molecular mechanisms underlying epigenetic inheritance, focusing on parental dietary and genetic perturbations affecting offspring phenotypes. Refining the methods for profiling epigenomes in sperm, we revealed the significant impact of cell-free DNA/chromatin contamination in prior studies. This enabled more accurate characterization of sperm epigenomes. Using a high-fat diet (HFD) exposure model, we demonstrated that metabolic phenotypes in offspring can be inherited from parents with metabolic disorders. Molecular analyses revealed paternal HFD effects had a stronger influence on early embryonic transcriptomes and chromatin states than maternal effects. Interestingly, HFD-induced chromatin alterations in sperm were largely erased in early embryos. Instead, changes in sperm small RNA payloads, particularly nuclear- and mitochondrial-derived tRNA fragments, were implicated as non-chromatin carriers of epigenetic inheritance. Using the X-linked gene Rlim, we developed a novel genetic model demonstrating that paternal Rlim knockout epigenetically transmitted an obesity resistance phenotype to offspring. Conditional Rlim knockout (cKO) pinpointed Sertoli cells as critical mediators of soma-germline communication, transferring epigenetic information to germ cells. RNA-seq analysis of Rlim cKO Sertoli cells identified Amh as a downstream target of this pathway. Profiling of Rlim cKO sperm further implicated nuclear- and mitochondrial- derived tRNA fragments as key epigenetic carriers, rather than chromatin accessibility or DNA methylation.