Kinase recruitment to membrane receptors is essential for signal transduction. However, the underlying regulatory mechanisms are poorly understood. We investigated how conformational changes control T cell receptor (TCR) association and activity of ZAP-70 kinase. Structural analysis of ZAP-70 showed that TCR binding or phosphorylation trigger transition from the closed/auto-inhibited conformation to an open conformation. Using ZAP-70 mutants with defined conformations, we found that TCR dwell-times control kinase activity. The auto-inhibited conformation minimizes receptor dwell-times and thereby avoids activation by membrane-associated kinases. Parallel recruitment of co-receptor-associated Lck kinase to the TCR ensures ZAP-70 phosphorylation and stabilizes ZAP-70 binding. Our study suggests that recruitment dynamics of cytosolic enzymes to the membrane regulate the activity and function of receptors lacking intrinsic catalytic activity.