Two contrasting theories have emerged that attempt to describe T-cell ligand potency, one based on the t_1/2 of the interaction and the other based on the equilibrium affinity (K_D). Here, we have identified and studied an extensive set of T-cell receptor (TCR)-peptide-MHC (pMHC) interactions for CD4⁺ cells that have differential K_Ds and kinetics of binding. Our data indicate that ligands with a short t_1/2 can be highly stimulatory if they have fast on-rates. Simple models suggest these fast kinetic ligands are stimulatory because the pMHCs bind and rebind the same TCR several times. Rebinding occurs when the TCR-pMHC on-rate outcompetes TCR-pMHC diffusion within the cell membrane, creating an aggregate t_1/2 (t_a) that can be significantly longer than a single TCR-pMHC encounter. Accounting for t_a, ligand potency is K_D-based when ligands have fast on-rates (k_on) and t_1/2-dependent when they have slow k_on. Thus, TCR-pMHC k_on allow high-affinity short t_1/2 ligands to follow a kinetic proofreading model.