Plants have an impressive repertoire to react to stress conditions that limit regular growth. Elevated temperatures beyond the optimal range cause rapid and specific transcriptional responses, resulting in developmental alterations and plasticity. Heat stress also causes chromatin decondensation and activation of some transposable elements (TEs), endangering genomic integrity. This is especially risky for stem cells in the shoot apical meristem (SAM) that potentially contribute to the next generation. We examined how the heat stress response in SAM stem cells of Arabidopsis (Arabidopsis thaliana) is different from that in other tissues and whether the elements of epigenetic TE control active in the meristem are involved in specific heat protection of stem cells. Using fluorescence-activated nuclear sorting to isolate and characterize SAM stem cells after exposure to conditions that activate a heat-responsive TE, we found that SAM stem cells maintain their developmental program and suppress the heat-response pathways dominating in surrounding somatic cells. Furthermore, mutants defective in DNA methylation recovered less efficiently from heat stress and persistently activated heat response factors and heat-responsive TEs. Heat stress also induced epimutations at the level of DNA methylation, especially in the CHG sequence context. Regions with modified DNA methylation patterns remained altered for at least 3†wk beyond the stress. These findings urge for disentangling cell type-specific responses under different stress types, especially for stem cells as bridges to the next generation.