Assessing the risk of unintended gene-editing effects is essential for therapeutic development but varies across stages of the pipeline (e.g., early candidate selection vs. late-stage safety assessment). UNCOVERseq (Unbiased Nomination of CRISPR Off-target Variants using Enhanced RhPCR) was recently introduced as an advanced in-cellulo workflow for sensitive off-target site nomination (<0.01% editing), offering defined input requirements and superior performance compared to existing methods for late-stage safety evaluation. Here, we present UNCOVERseq-pools, a modified, highly multiplexed version optimized for rapid assessment during early candidate selection. Using equimolar pooled gRNAs (< 20 gRNAs) in a promiscuous editing system, UNCOVERseq-pools maintains the high sensitivity of UNCOVERseq (>95% off-target event capture) across diverse gRNAs. We further improve the workflow computationally by incorporating a decontamination algorithm (CATCH), demonstrating further improvements to specificity with minimal impacts on sensitivity. Finally, by implementing UNCOVERseq-pools as a batch-executed, community-accessible service, we provide an economical solution for empirical off-target nomination across varied safety assessment needs. Overall, UNCOVERseq and its pooled variant enhance informed risk assessment in translational gene-editing systems by improving both the quality and accessibility of off-target detection workflows.