In sexual reproduction, maternally inherited small RNAs are crucial for embryo development, whereas the role of sperm-borne small RNAs remains unclear. Previous studies on paternal small RNA inheritance reported highly variable sperm RNA profiles and relied on correlational evidence, leaving technical and mechanistic questions unresolved. Using optimized sequencing approaches, we revisited sperm small RNA composition and showed that mature sperm retain a selected subset of spermatogenic species. During sperm maturation, cytoplasmic species undergo extensive depletion, while highly abundant pachytene PIWI-interacting RNAs (piRNAs) are preferentially retained and remain stable during capacitation. We further show that in sperm, piRNAs are associated with the PIWI protein MIWI. Focusing on pi6 piRNAs—a pachytene piRNA population linked to intergenerational effects—we identify a subset of sperm-specific sequences present in early embryos. Transcriptomic analysis of paternal pi6 mutant embryos identified dysregulation of genes involved in oxidative phosphorylation, suggesting that pi6 piRNAs may influence embryonic metabolic pathways.