Barn owls experience increasing interaural time differences (ITDs) during development, because their head width more than doubles in the month after hatching. We therefore hypothesized that their ITD detection circuit might be modified by experience. To test this, we raised owls with unilateral ear inserts that delayed and attenuated the acoustic signal, then used the binaural neurophonic to measure ITD representation in the brainstem nucleus laminaris (NL) when they were adult. The ITD circuit is composed of delay line inputs to coincidence detectors, and we predicted that plastic changes would lead to shorter delays in the axons from the manipulated ear, and complementary shifts in ITD representation on the two sides. In owls that received ear inserts around P16, the maps of ITD shifted in the predicted direction, but only on the ipsilateral side, and only in those regions that had not experienced auditory stimulation prior to insertion. The contralateral map did not change. Thus, experience-dependent plasticity of the ITD circuit occurs in NL, and our data suggest that ipsilateral and contralateral delays are independently regulated. Thus, altered auditory input prior to, and during, sensory experience leads to long lasting changes in the representation of ITD.