Technical Abstract: /Cis/-nat-siRNAs are a recently characterized class of small regulatory RNAs that are widespread in eukaryotes. Despite their abundance the importance of their regulatory activity is largely unknown. The only functional role for eukaryotic /cis/-nat-siRNAs that has been described to date is in environmental stress responses in plants. Here we demonstrate that /cis/-nat-siRNA-based regulation plays key roles in Arabidopsis reproductive function, as it facilitates both gametophyte formation and double fertilization, a developmental process of enormous agricultural value. We show that male gametophytic /kokopelli/ (/kpl/) mutants display frequent single fertilization events, and that /KPL/ and a inversely transcribed gene, /ARIADNE14 (ARI14)/, which encodes a putative ubiquitin-E3 ligase, generate a sperm-specific nat-siRNA pair. In the absence of /KPL/, /ARI14/ RNA levels in sperm are increased and fertilization is impaired. Furthermore,/ ARI14/ transcripts accumulate in several siRNA biogenesis pathway mutants and over-expression of /ARI14 /in sperm/ /phenocopies the reduced seed set of the /kokopelli/ mutants. These results extend the regulatory capacity of /cis/-nat-siRNAs to development by identifying a role for /cis/-nat-siRNAs in controlling sperm function during double fertilization.