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Understanding how plants adapt to ambient temperatures has become a major challenge prompted by global climate change. This has led to the identification of several genes regulating the thermal plasticity of plant growth and flowering time. However, the mechanisms accounting for the natural variation and evolution of such developmental plasticity remain mostly unknown. In this study, we determined that natural variation at ICARUS2 (ICA2), which interacts genetically with its homolog ICA1, alters growth and flowering time plasticity in relation to temperature in Arabidopsis (Arabidopsis thaliana). Transgenic analyses demonstrated multiple functional effects for ICA2 and supported the notion that structural polymorphisms in ICA2 likely underlie its natural variation. Two major ICA2 haplogroups carrying distinct functionally active alleles showed high frequency, strong geographic structure, and significant associations with climatic variables related to annual and daily fluctuations in temperature. Genome analyses across the plant phylogeny indicated that the prevalent plant ICA genes encoding two tRNA(His) guanylyl transferase 1 units evolved similar to 120 million years ago during the early divergence of mono- and dicotyledonous clades. In addition, ICA1/ICA2 duplication occurred specifically in the Camelineae tribe (Brassicaceae). Thus, ICA2 appears to be ubiquitous across plant evolution and likely contributes to climate adaptation through modifications of thermal developmental plasticity in Arabidopsis.