Orientation is one of the most salient features in visual scenes. Neurons at multiple levels of the visual system detect orientation, but in many cases the underlying biophysical mechanisms remain unresolved. Here, we study the mechanism for orientation detection at the earliest stage in the visual system, in B/K wide-field amacrine cells (B/K WACs), a novel group of giant, non-spiking interneurons in the mouse retina. B/K WACs exhibit orientation-selective calcium signals along their long, straight, unbranching dendrites, which contain both synaptic inputs and outputs. In this study, we identify the key computational strategy, termed 'compartmentalized pooling,' that generates orientation selectivity in B/K WAC dendrites. To characterize the geometry of the dendritic receptive field of B/K WACs, we performed simultaneous dendritic calcium imaging and somatic voltage recordings. Comparison of the two signals shows that individual B/K dendrites are electrotonically isolated, exhibiting a spatially confined yet extended receptive field along the preferred orientation (PO) axis, which we term ‘compartmentalized pooling.’ Further, the receptive field of the B/K WAC dendrite exhibits center-surround antagonism along the null orientation (NO) axis. Phenomenological receptive field models demonstrate that compartmentalized pooling generates orientation selectivity, while center-surround antagonism shapes band-pass spatial frequency tuning. At the microcircuit level, B/K WACs receive excitation driven by one contrast polarity (e.g., ‘ON’) and glycinergic inhibition driven by the opposite polarity (e.g., ‘OFF’). However, this ‘push-pull’ inhibition is not essential for generating orientation selectivity. A minimal biophysical model reproduces compartmentalized pooling from feedforward excitatory inputs combined with a substantial increase in the specific membrane resistance between somatic and dendritic compartments.  Collectively, our results reveal the biophysical principles underlying dendritic computation of orientation in B/K WACs, advancing our understanding of the diverse strategies employed throughout the visual system to detect orientation.