Recent research has established that catabolic conversions within the jasmonate pathway have significant consequences on hormone signaling output. In dicotyledonous plants, the jasmonic acid oxidase (JAO) catabolic route is endowed with a regulatory function by diverting jasmonic acid (JA) towards hydroxylation, at the expense of its conjugation into the bioactive jasmonoyl-isoleucine (JA-Ile) hormone. Here we functionally characterized the JAO pathway in rice (Oryza sativa) and demonstrate its prevalent function in promoting growth and attenuating JA responses in vegetative tissues. The rice genome contains four JAO-related homologs of which three generated hydroxy-JA in vitro and reverted the high defense phenotype when expressed in the Arabidopsis jao2-2 mutant. By generating and analyzing a series of single to quadruple rice jao mutants, we show the incremental effect of gradual JAO depletion on JA metabolism, basal defense levels, growth inhibition, fitness and global metabolic reprogramming. JAO-deficient lines were significantly growth-retarded at the juvenile stage, while recovering a near wild-type vegetative development after three months, where they exhibited a enhanced resistance to virulent and avirulent strains of Magnaporthe oryzae, the causal agent of fungal blast disease. Our findings identify the JAO pathway as an integral component of rice JA homeostasis and an important determinant of the growthdefense tradeoff. They demonstrate its conserved regulatory function in monocots and open possibilities for modulating selectively basal JA responses in a major cereal crop. Natural variation in JAO activity could also be explored as a mechanism underlying varying levels of JA signaling output in rice.