Legumain (or asparaginyl endopeptidase) is mainly known as a lysosomal protease with very narrow specificity cleaving peptide substrates after Asn residues. However, in acidic environments this protease similar to the caspases also recognizes substrates with Asp in the P1 position. Legumain activity is crucial for maintaining cellular homeostasis and legumain up-regulation is linked to diseases like inflammation, arteriosclerosis and tumorgenesis. Thus legumain is an excellent molecular target for the development of new potent and selective small molecule chemical markers. Here, the previously established Hybrid Combinatorial Substrate Library (HyCoSuL) approach incorporating unnatural amino acids in the peptide scaffold was used for the development of biotin-labeled acyloxymethyl ketone (AOMK) inhibitors with Asp in the P1 position targeting legumain but not caspases. The specificity of these probes was validated using a stable monoclonal legumain over-expressing HEK293 (M38L) cell line and a cytochrome c-triggered apoptosis model of FreeStyle 293-F cell extracts. The new compounds developed in this study might be used for tracking active legumain in various biological models in which caspases are also active.