Biomolecular condensates are cellular compartments without enveloping membranes, enabling them to dynamically adjust their composition in response to environmental changes through post-translational modifications. A recent study has revealed that interferon-induced ADP-ribosylation (ADPr), which can be reversed by a SARS-CoV-2-encoded hydrolase, is enriched within a condensate. However, the identity of the condensate and responsible host ADP-ribosyltransferase remain elusive. Here, we demonstrate that interferon induces ADPr through transcriptional activation of PARP14, requiring both its physical presence and catalytic activity for condensate formation. Interferon-induced ADPr colocalizes with PARP14 and its protein-level regulator DTX3L, and these PARP14/ADPr condensates contain key components of p62 bodies—including the selective autophagy receptor p62 and its binding partners NBR1 and TAX1BP1, along with K48-linked and K63-linked polyubiquitin chains—but lack the autophagosome marker LC3B. Knockdown of p62 disrupts the formation of these ADPr condensates. Importantly, these structures are unaffected by autophagy inhibition but depend on ubiquitin-activating enzyme E1, E3 ligase DTX3L, and proteasome activity. Taken together, these findings demonstrate that interferon triggers PARP14-mediated ADP-ribosylation in p62 bodies, which requires an active ubiquitin-proteasome system.