The primary visual cortex of primates and carnivores is organized into columns of neurons with similar preferences for stimulus orientation, but the developmental origin and function of this organization are still matters of debate. We found that the orientation preference of a cortical column is closely related to the population receptive field of its ON and OFF thalamic inputs. The receptive field scatter from the thalamic inputs was more limited than previously thought and matched the average receptive field size of neurons at the input layers of cortex. Moreover, the thalamic population receptive field (calculated as ON - OFF average) had separate ON and OFF subregions, similar to cortical neurons in layer 4, and provided an accurate prediction of the preferred orientation of the column. These results support developmental models of orientation maps that are based on the receptive field arrangement of ON and OFF visual inputs to cortex.