Navigating through a vivid environment requires animals to rapidly process a bewildering mass of sensory signals and interpret it in the context of ongoing behavior. Local and global motion cues along with luminance information guide them to orient and interact adaptively within the world. Larval zebrafish react to such signals with behaviors ranging from active light seeking and shadow avoidance to optomotor swimming or hunting that are expressed in kinematically distinct movements. We asked how are the brain-wide networks of neurons organized that process such signals and how do they integrate information across visual space and time?We recorded neuronal activity dynamics to a diverse set of behaviorally relevant stimuli, including whole-field motion, prey-like and threatening stimuli using high-resolution two-photon and fast volumetric light-sheet microscopy. Molecular profiling of functionally identified classes and registration to a common brain reference allowed us to build an integrated map that combines functional organization and genetic identity. In early visual processing centers, we correlated neuronal function with the expression of developmental marker genes and neurotransmitter or neuromodulator specificity to uncovered how visual and behavioral signals are integrated in evolutionary conserved thalamic and pretectal nuclei. Brain-wide activity dynamics to such visual cues were dissected by imaging from genetically targeted populations of neurons using a variety of cell-type-specific GAL4 lines. Our data provide insight in key constraints to circuit models for spatial orientation, and genetic entry points for circuit analysis and manipulation.