Abstract In plants, small-interfering RNAs (siRNAs) are mainly produced from transposable elements (TEs) within the RNA-directed DNA methylation pathway (RdDM), which is particularly important during reproductive development in many plant species. However, there is limited understanding of the origins, dynamics and function of TE-derived siRNAs acting in different cellular and developmental contexts. Here, we used the RNaseIII-like protein RTL1 to suppress siRNA biogenesis specifically in Arabidopsis pollen, and found distinct siRNA subsets produced in the sperm and vegetative cell lineages via RNA polymerase IV (Pol IV). We show that gametophytic siRNAs produced in the vegetative cell reinforce RdDM in pollen and interploidy hybridization barriers in the seed, while siRNAs produced specifically in sperm cells do not impact the epigenome and are dispensable for the “triploid block”. These results demonstrate that active siRNA biogenesis in the two pollen cell types has contrasting roles in transposon silencing and transgenerational epigenetic inheritance.