Global excitatory activity patterns across the dorsal cortex are reorganized when mice perform perceptual decision-making tasks that involve different underlying computations and vary in complexity. However, the circuit mechanisms enabling such large-scale activity reorganization remain unknown. An interesting possibility is that they depend on neuromodulatory input to the cortex. In particular, cholinergic neurons in the basal forebrain project widely across cortical areas while exhibiting topographical and functional heterogeneity. They are therefore well equipped to serve as an orchestrator of large-scale task-dependent cortical activity. To test this hypothesis, we first measured cholinergic-axon dynamics with widefield imaging from across the dorsal cortex of mice performing a cued task-switching paradigm in virtual reality, with dozens of unpredictable switches within a session. Specifically, they rapidly switched between a complex task that requires gradual evidence accumulation over time and a simple task where the correct choice on each trial is indicated by a salient visual cue. We observed stronger cholinergic activity throughout the cortex during evidence accumulation in the complex task compared to the simple task. In addition, the animals’ choice could be decoded from cortex-wide cholinergic activity. To investigate whether cholinergic input is required for task-specific computations, we virally expressed the red-shifted inhibitory opsin Jaws bilaterally in the basal forebrain. We then optically silenced cholinergic terminals across the cortex during evidence accumulation, while measuring large-scale cortical excitatory activity with widefield GCaMP6s imaging. Strikingly, inhibiting cholinergic input to the cortex selectively reduced performance of the complex task. Furthermore, silencing cholinergic terminals impaired cortical coding of accumulated evidence, and attenuated activity decorrelation across cortical areas specifically in the complex task. Our findings offer compelling evidence for cortex-wide cholinergic input serving as a novel, parsimonious circuit mechanism sculpting cognitive computation across the cortex in a task-dependent manner.