The control of mRNA stability is a key determinant of gene expression in eukaryotes. Although XRN4, the plant cytoplasmic 5’ to 3’ exoribonuclease, plays a central role in mRNA degradation in Arabidopsis, plants lacking the enzyme appear relatively normal. We sought to identify substrates of XRN4 and use this information to identify functional impacts of the enzyme at the whole plant level. The substrates were identified by assaying the population of partially degraded mRNAs (the RNA degradome) in WT and xrn4 mutants. Both polyadenylated and nonpolyadenylated RNA degradomes were investigated because many XRN4 substrates are likely first deadenylated. We then identified functional groups enriched among XRN4 substrates to hypothesize which processes XRN4 is important for, with responses to environmental stress being of particular interest. This approach led to the discovery that XRN4 is critical for normal responses to prolonged darkness and during recovery from nitrogen starvation. Beyond demonstrating these new roles for XRN4, the results of this work also expand understanding of the contribution of XRN4 to nonsense-mediated mRNA decay and uncover an unexpected facet of the process in Arabidopsis.