Arbuscular mycorrhizal (AM) symbiosis modulates plant-herbivore interactions. Still, how it shapes the overall plant defense strategy and the mechanisms involved remain unclear. We investigated how AM symbiosis simultaneously modulates plant resistance and tolerance to a shoot herbivore, and explored the underlying mechanisms. Bioassays with Medicago truncatula plants were used to study the effect of the AM fungus Rhizophagus irregularis on plant resistance and tolerance to Spodoptera exigua herbivory. By performing molecular and chemical analyses, we assessed the impact of AM symbiosis on herbivore-triggered phosphate (Pi)- and jasmonate (JA)-related responses. Upon herbivory, AM symbiosis led to an increased leaf Pi content by boosting the mycorrhizal Pi-uptake pathway. This enhanced both plant tolerance and herbivore performance. AM symbiosis counteracted the herbivore-triggered JA burst, reducing plant resistance. To disentangle the role of the mycorrhizal Pi-uptake pathway in the plant´s response to herbivory, we used the mutant line ha1-2, impaired in the H+ -ATPase gene HA1, which is essential for Pi-uptake via the mycorrhizal pathway. We found that mycorrhiza-triggered enhancement of herbivore performance was compromised in ha1-2 plants. AM symbiosis thus affects the defense pattern of M. truncatula by altering resistance and tolerance simultaneously. We propose that the mycorrhizal Pi-uptake pathway is involved in the modulation of the plant defense strategy. This article is protected by copyright. All rights reserved.