Telomere length has been implicated in the organismal response to stress, but the underlying mechanisms are unknown. Here we examine the impact of telomere length changes on Arabidopsis thaliana responses to three contrasting abiotic environments, and measure 31 fitness, development, physiology and leaf-level anatomy traits. We report that telomere length in wild type and short telomere mutants is resistant to abiotic stress, while elongated telomeres in ku70 mutants are more plastic. We also detect significant pleiotropic effects of telomere length on flowering time and key leaf physiology and anatomical traits. Furthermore, our data reveal a significant genotype by environment (GxE) interaction for reproductive fitness, with the benefits and costs to performance depending on the growth conditions. These results imply that life-history tradeoffs between flowering time and reproductive fitness are impacted by telomere length variation. We postulate that telomere length in plants is subject to natural selection imposed by different environments.