Communication among neocortical areas is largely thought to be mediated by long-range synaptic interactions between cortical neurons, with the thalamus providing only an initial relay of information from the sensory periphery. Higher-order thalamic nuclei receive strong synaptic inputs from the cortex and send robust projections back to other cortical areas, providing a distinct and potentially critical route for corticocortical communication. However, the relative contributions of corticocortical and thalamocortical inputs to higher-order cortical function remain unclear. Using imaging of neurons and axon terminals in combination with optogenetic manipulations, we find that the higher-order visual thalamus of mice has a unique impact on the posterior medial visual cortex (PM). Whereas corticocortical projections from lower cortical areas convey robust visual information to PM, higher-order thalamocortical projections convey information about global arousal state. Together, these findings suggest a key role for the higher-order thalamus in providing contextual signals that may flexibly modulate cortical sensory processing.