Exocytosis of synaptic vesicles is rapidly followed by compensatory plasma membrane endocytosis. The efficiency of endocytosis varies with experimental conditions, but the molecular basis for this control remains poorly understood. Here, the function of dynamin 1, the neuron-specific member of a family of GTPases implicated in vesicle fission, was investigated with high temporal resolution via membrane capacitance measurements at the calyx of Held, a giant glutamatergic synapse. Endocytosis at dynamin 1 KO calyces was the same as in wild type after weak stimuli, consistent with the nearly normal ultrastructure of mutant synapses. However, following stronger stimuli, the speed of slow endocytosis, but not of other forms of endocytosis, failed to scale with the increased endocytic load. Thus, high level expression of dynamin 1 is essential to allow the slow, clathrin-mediated endocytosis, which accounts for the bulk of the endocytic response, to operate efficiently over a wide range of activity.