Genome amplification and sequence divergence provides raw materials to allow organismal adaptation. This is exemplified by the large expansion of the ubiquitin-26S proteasome system (UPS) in land plants, which primarily rely on intracellular signaling and biochemical metabolism to combat biotic and abiotic stresses. While a handful of functional genomic studies have demonstrated the adaptive role of the UPS in plant growth and development, many UPS members remain unknown. In this work, we applied a comparative genomic study to address the functional divergence of the UPS at a systematic level. We first used a closing-target-trimming annotation approach to identify most, if not all, UPS members in six species from each of two evolutionarily distant plant families, Brassicaceae and Poaceae. To reduce age-related errors, the two groups of species were selected based on their similar chronological order of speciation. Through size comparison, chronological expansion inference, evolutionary selection analyses, duplication mechanism prediction, and functional domain enrichment assays, we discovered significant diversities within the UPS, particularly between members from its three largest ubiquitin ligase gene families, the F-box (FBX), the Really Interesting New Gene (RING), and the Bric-a-Brac/Tramtrack/Broad Complex (BTB) families, between Brassicaceae and Poaceae. Uncovering independent Arabidopsis and Oryza genus-specific subclades of the 26S proteasome subunits from a comprehensive phylogenetic analysis further supported a diversifying evolutionary model of the UPS in these two genera, confirming its role in plant adaptation.