Deubiquitinating enzymes (DUBs) play important roles in maintaining cellular protein homeostasis through the regulation of ubiquitination. They are being increasingly considered as drug targets, with DUB inhibitors currently being tested in clinical trials for the treatment of cancer and neurodegeneration. Activity-based probes (ABPs) formed of ubiquitin for DUB specificity, and a cysteine reactive warhead can inform on inhibitor potency, selectivity, cellular permeability and target engagement in a cellular environment with endogenous DUB expression. Tagged DUB ABPs can be used to immunoprecipitate DUB-ABP complexes for subsequent analysis via mass spectrometry-based proteomics. We have successfully translated the ABP immunoprecipitations to a 96 well plate format via multiple automated and manual methodologies, and have matched the throughput of this with 100 sample per day methodology on a timsTOF-Evosep LC-MS/MS. The application of data-independent acquisition PASEF increased the depth of the DUBome identified by this higher-throughput methodology. Implementation of the methodology to screen a selected library of small molecules predicted to react with cysteines has revealed novel DUB inhibitors for USP47/7, OTUD7B (Cezanne) and USP5. Follow up functional validations indicate these compounds could be used as scaffolds to further develop potent DUB inhibitors, or used as tools to study the activity of these potential drug targets in cells.