Flavivirus subgenomic RNAs (sfRNAs) antagonise antiviral defences, yet how sfRNAs are organised and maintained in cells remains poorly understood. Here we identify ubiquitin C-terminal hydrolase L3 (UCHL3) as a post-translational regulator of flavivirus sfRNA stability and function. Using a proximity-biotinylation sfRNA-interactome capture strategy (sfRAPID), we systematically identified sfRNA-interacting proteins during Zika virus infection. The engineered sfRNA construct contains flanking BoxB stem-loop structures that recruit a BirA-λN fusion protein (BASU), enabling biotinylation of proteins in close proximity to sfRNA and their subsequent isolation using streptavidin-conjugated beads. LC-MS/MS analysis of streptavidin pulldowns identified RNA-granule scaffolds and enzymes significantly enriched in sfRNA complexes relative to control RNA, including G3BP1, DDX10, DDX3, UBAP2L, OTUD4, RNase L, and UCHL3. This dataset provides an unbiased catalogue of the sfRNA-associated proteome during flavivirus infection, revealing that UCHL3 is incorporated into sfRNA-containing ribonucleoprotein assemblies where it functions as a proviral factor by suppressing RNase L activation and maintaining sfRNA within protective P-body compartments.