Cognitive flexibility involves adapting behaviour to changing rules or contexts by modifying input-output mappings of brain-wide networks to achieve context-appropriate behaviour. This process relies on distinct neural representations of different rules or contexts in multiple brain regions, as well as changes in functional connectivity across brain regions. While context-dependent changes in neural responses have been studied locally in various brain regions, it is not clear to what extent different contexts lead to changes in functional connectivity between brain regions. We imaged widefield calcium activity from the entire dorsal cortex of mice as they switched between two distinct contexts in an attention-switching task. Different task contexts were distinctly represented across multiple cortical areas with both increases and decreases in average activity levels, which could not be accounted for by overt movements. These average activity changes were observed in both sensory and motor areas and were present both during baseline and stimulus-evoked periods. We performed locally selective spectral clustering to segment the cortex into functional parcels and used correlations in activity between these functionally defined regions to obtain measures of cortex-wide functional connectivity. Different task contexts were associated with widespread, systematic changes in functional connectivity. While some regions showed uniform, cortex-wide changes in functional connectivity, the majority of regions showed a heterogenous distribution of increased and decreased functional connectivity distributed across different brain regions. Interestingly, during visual attention, visual and retrosplenial cortex showed the greatest increase in functional coupling to most other regions of the brain. These results demonstrate that changes in mesoscale functional connectivity provide a substrate for flexibly rerouting information across brain-wide networks with changing contextual demands.