The cAMP-PKA signalling cascade in budding yeast regulates adaptation to changing environments. Many questions remain about the function of cAMP dynamics, largely because no robust method for in vivo cAMP measurements exists for yeast. Here we developed yEPAC, a FRET-based biosensor for cAMP measurements in yeast. We show that this biosensor can be used in flow cytometry, allowing for highthroughput single cell-level quantification that complements microscopy measurements. We quantified both steady-state cAMP levels and dynamic changes in response to sudden nutrient transitions. Steadystate cAMP levels were found to correlate with growth rate (rather than glycolytic flux) and were independent of extracellular sensing. During transitions, a cAMP-peak differentiates between different carbon source transitions, and is generated only when switching from non-or slowly-fermentable sugars to rapidly fermentable ones. Furthermore, generation of the cAMP peak is mediated by a combination of extracellular sensing and metabolism; deficits in either results in a largely diminished response. Moreover, the cAMP peak follows Weber's law; its height scales with the relative, and not the absolute, change in glucose. This means that cells respond to small changes in extracellular glucose when the initial level is low, but ignore these changes when this level is high. Lastly, we speculate that the cAMP peak height conveys information about prospective growth rates, especially for fermentable sugars. In conclusion, our yEPAC-sensor makes possible new avenues for understanding yeast physiology, signalling and metabolic adaptation.