Regulatory non-coding RNAs include small RNAs (smRNAs) that are 20 - 40 nucleotides in length and long non-coding RNAs (lncRNAs) that exceed 200 nucleotides. In Arabidopsis thaliana, smRNAs are typically generated from long double-stranded RNA molecules produced by one of the six RNA-dependent RNA Polymerase (RDR) proteins, while lncRNAs are transcribed by RNA polymerase II and may be regulated by transcription factors (TFs). These ncRNAs play crucial roles in stress tolerance and can regulate the plant hormone abscisic acid (ABA) signaling pathway, which is a major regulator of plant responses to abiotic stressors. However, there are gaps in our understanding regarding the regulation of smRNA biogenesis that is mediated by RDRs, the potential role of RDR-dependent smRNAs in plant response to abiotic stresses, and whether lncRNAs whose transcription is regulated by ABA-triggered transcription factors binding sites are required for proper plant response to the plant hormone ABA. To address these questions, we first performed a global genomic analysis to identify the first known substrates for Arabidopsis thaliana RDR3, 4, and 5, which were not previously defined. We also identified new substrates for RDR1, 2, and 6, as well as the co-factors for RDR2 and RDR6, RNA-DIRECTED DNA METHYLATION 12 (RDM12) and SUPRESSOR OF GENE SILENCING 3 (SGS3), respectively. Our findings indicate that SGS3 substrates are not limited to those exclusively utilized by RDR6, but that this protein seems to serve as a more general co-factor for all plant RDR proteins. Furthermore, we discovered that RDR6 and SGS3 are involved in silencing transcripts associated with abiotic stresses, including ABA response, water deprivation, and salt stress. Secondly, we screened lncRNAs potentially regulated by ABA-induced TFs under exogenous ABA treatment, and found that when some of these lncRNAs are mutated the resulting mutant plants exhibited hyposensitive/hypersensitive phenotypes to this hormone, indicating their potential involvement in regulating ABA responses in Arabidopsis thaliana. Deciphering the molecular mechanisms underlying abiotic stress responses in plants is important, since this knowledge can guide us to enhance crop survival in increasingly extreme environments. Our study reveals previously unexplored mechanisms in the RDR6/SGS3-dependent RNA silencing pathway and unknown functions of lncRNAs in plant abiotic stress responses.