Cellular energetic status depends on a balance of nutrient catabolism and biosynthesis, orchestrated by a regulatory network centered on the kinases mTOR and AMPK. This network is integrated with growth factor signaling, including RAS/ERK and PI3K/AKT, which operate dynamically as they adjust to a cell’s changing nutrient availability and regulatory microenvironment. We have developed a live-cell imaging approach to probe metabolic and signaling states in parallel, combining biosensors for ATP concentration, ADP/ATP ratio, and glycolytic intermediates with reporters for AMPK, AKT, mTOR and ERK kinase activity. With this approach, we observe a range of dynamic activities, which vary depending on the level of metabolic stress. Our results indicate that proliferative signaling programs can be temporally gated by phases of catabolic activity and suggest that a loss of intracellular pathway coordination may contribute to cellular dysfunction under pathological conditions.