The role played by phytohormone signaling in the modulation of DNA repair gene and the resulting effects on plant adaptation to genotoxic stress are poorly investigated. Information has been gathered using the Arabidopsis ABA (abscisic acid) overly sensitive mutant abo4-1, defective in the DNA polymerase ε function that is required for DNA repair and recombination. Similarly, phytohormone-mediated regulation of the Ku genes, encoding the Ku heterodimer protein involved in DNA repair, cell cycle control and telomere homeostasis has been demonstrated, highlighting a scenario in which hormones might affect genome stability by modulating the frequency of homologous recombination, favoring plant adaptation to genotoxic stress. Within this context, the characterisation of Arabidopsis AtKu mutants allowed disclosing novel connections between DNA repair and phytohormone networks. Another intriguing aspect deals with the emerging correlation between plant defense response and the mechanisms responsible for genome stability. There is increasing evidence that systemic acquired resistance (SAR) and homologous recombination share common elements represented by proteins involved in DNA repair and chromatin remodeling. This hypothesis is supported by the finding that volatile compounds, such as methyl salicylate (MeSA) and methyl jasmonate (MeJA), participating in the plant-to-plant communication can trigger genome instability in response to genotoxic stress agents. Phytohormone-mediated control of genome stability involves also chromatin remodeling, thus expanding the range of molecular targets. The present review describes the most significant advances in this specific research field, in the attempt to provide a better comprehension of how plant hormones modulate DNA repair proteins as a function of stress.