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Fitness tradeoffs between different environments enable the maintenance of microbial diversity. While the importance of tradeoffs is clear, it has been surprisingly difficult to predict which traits they will occur between and at how granular a level. For example, it is unclear whether performance between a constant versus pulsed exposure of the same stress tends to be positively correlated, independent of each other, or negatively correlated. Empirically, it has been shown that a critical feature structuring microbial communities is temperature. However, the compatibility between strategies to deal with different forms of heat stress is unclear. For instance, are strains that grow well at higher temperatures also stronger at withstanding heat shock? To understand how environmental microbes can adapt to better deal with heat stress, we performed an evolution experiment using a dominant phyllosphere microbe <i>Methylobacterium extorquens</i> in a regime of intermittent heat shock. We identified the genetic basis of adaptation, discovering a large number of loci capable of mediating adaptation to heat shock, many of which had not been previously linked to heat stress. Despite the genetic divergence among evolved isolates, we discovered a general tradeoff between heat shock resistance and growth at consistently elevated temperatures. We found this tradeoff was not limited to evolved isolates, but also represented across a sample of environmentally isolated <i>Methylobacterium</i> strains. These findings indicate a generic conflict between strategies to deal with heat shock recovery and growth at elevated temperatures, suggesting even variation in intensities of a stressor can drive diversity in microbial strategies.IMPORTANCEOne of the key forces shaping the microbial diversity in nature is temperature. However, temperature in ecological settings is variable, and it is unknown if strategies to deal with different intensities of high temperature are compatible or not. Using evolution experiments, we identify the genetic basis of adaptation to heat shock in <i>Methylobacterium extorquens</i>, a dominant member of the phyllosphere microbiome. We discover a number of genetic targets where beneficial mutations improve heat shock resistance, most of which have not been implicated with heat stress before. For both the evolved isolates and a set of environmentally isolated <i>Methylobacterium</i> strains, we discover a general tradeoff between recovery after heat shock and growth at elevated temperatures. While the strategies to deal with increasing temperatures have garnered significant interest, our results suggest that even different intensities of heat stress can select for distinct and incompatible strategies and can drive microbial diversification in ecological settings.