The granular retrosplenial cortex (RSG) is critical for both spatial navigation and fear conditioning, but the neural codes enabling these seemingly disparate functions remain unknown. Here, using optogenetic circuit mapping, we reveal a double dissociation that allows parallel circuits in superficial RSG to process navigation- versus fear-related inputs. The anterior thalamus, a source of head direction information, strongly recruits small, low rheobase (LR) pyramidal cells in RSG layer 3. Neighboring regular-spiking (RS) cells are instead preferentially controlled by claustral and anterior cingulate inputs, sources of higher-order and fear-related information. Precise sublaminar axonal and dendritic arborization within RSG layer 1 enable this parallel processing. Synaptic dynamics and computational modeling suggest LR neurons are optimally-tuned conjunctive encoders of direction and distance inputs from the thalamus and dorsal subiculum, respectively. RS cells are better positioned to support contextual fear memories. Thus, parallel input streams to computationally-distinct principal neurons help facilitate diverse RSG functions.