Seed germination plays a vital role in ensuring plant survival under unfavorable conditions. Abscisic acid (ABA) signaling is important for integrating environmental information to regulate seed germination. Despite the identification of numerous regulatory factors in ABA signaling pathways during seed germination, the transcriptional regulatory mechanisms influencing ABA signaling remain largely uncharacterized. Long non-coding RNAs (lncRNAs) have many physiological functions in diverse organisms. To date, only a few seed germination-related lncRNAs have been reported. The AtR8 lncRNA (259 nt) in Arabidopsis is transcribed by the RNA polymerase III. We previously determined that the AtR8 lncRNA affects the innate immunity of seedlings as well as hypocotyl elongation. It is also highly expressed in the germinating seeds and induced by ABA. In this study, its loss-of-function mutant (atr8) had incompletely formed siliques and seeds and a relatively low germination rate. The germination efficiency and primary root elongation were strongly affected by the ABA level. In addition, ABA signaling and AtEM6 expression were significantly induced in the atr8 mutant. Moreover, the AtEM6-overexpressing Arabidopsis plants and the atr8 mutant had similar ABA-dependent phenotypes. Genetic analyses clarified the relationship between AtR8 and AtEM6 during ABA signaling. The stress-dependent transcription of WRKY46 in the germinating atr8 seeds was significantly upregulated by ABA. AtEM6 expression increased in a wrky46 background. WRKY46 promoted AtEM6 expression by binding to the gene promoter W-boxes in a yeast one-hybrid assay. These results suggest the AtR8 lncRNA integrates WRKY46 into the ABA signaling pathway to regulate AtEM6 expression and influences seed germination and silique development in Arabidopsis. The study elucidated the mechanism of AtR8 lncRNA in regulating seed germination and seedling growth through mediate ABA signaling.