Cells use information about their environments and internal states to decide whether to proliferate, differentiate, or enter non-proliferative states such as quiescence and senescence. But how do they integrate this information to make unambiguous decisions? Here, we describe how the interaction between two independent condensates, P-bodies and Whi3-dependent condensates, enables individual yeast cells to integrate information about their biological age and the presence of potential mates during fate decisions. Both formation and interaction of these condensates were necessary and sufficient to drive old cells into senescence and store age information in the yeast mother cell at mitosis. This same network also primed old cells to choose proliferation over mating when exposed to mating pheromone, demonstrating that it injects contextual information into multiple decisions. Thus, biomolecular condensates and their interactions can collect and integrate contextual information to adjust cellular decisions to overlapping life events.