Structural adaption in living systems is achieved by competing catalytic pathways that drive assembly and disassembly of molecular components under the influence of chemical fuels. We report on a simple mimic of such a system that displays transient, sequence‐dependent formation of supramolecular nanostructures based on biocatalytic formation and hydrolysis of self‐assembling tripeptides. The systems are catalyzed by α‐chymotrypsin and driven by hydrolysis of dipeptide aspartyl‐phenylalanine‐methyl ester (the sweetener aspartame, DF‐OMe). We observed switch‐like pathway selection, with the kinetics and consequent lifetime of transient nanostructures controlled by the peptide sequence. In direct competition, kinetic (rather than thermodynamic) component selection is observed. Off the beaten track: Sequence‐dependent kinetic pathway selection in chemically fueled catalytic self‐assembly of tripeptides is demonstrated, in which the control of the lifetime of the nanostructures is dictated by chemical design. Mimicking the unique features of these systems may open up opportunities to create supramolecular systems for non‐equilibrium motility and shape control.