Biological visual systems have the remarkable ability to recognize objects despite confounding factors such as object position, size, pose, and lighting. In primates, this ability likely results from neuronal responses at the highest stage of the ventral visual stream [inferior temporal cortex (IT)] that signal object identity while tolerating these factors. However, for even the apparently simplest IT tolerance (“invariance”), tolerance to object position on the retina, little is known about how this feat is achieved. One possibility is that IT position tolerance is innate in that discriminatory power for newly learned objects automatically generalizes across position. Alternatively, visual experience plays a role in developing position tolerance. To test these ideas, we trained adult monkeys in a difficult object discrimination task in which their visual experience with novel objects was restricted to a single retinal position. After training, we recorded the spiking activity of an unbiased population of IT neurons and found that it contained significantly greater selectivity among the newly learned objects at the experienced position compared with a carefully matched, non-experienced position. Interleaved testing with other objects shows that this difference cannot be attributed to a bias in spatial attention or neuronal sampling. We conclude from these results that, at least under some conditions, full transfer of IT neuronal selectivity across retinal position is not automatic. This finding raises the possibility that visual experience plays a role in building neuronal tolerance in the ventral visual stream and the recognition abilities it supports.