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Extracellular adenosine 5′‐triphosphate (eATP) is an essential signaling molecule that mediates different cellular processes through its interaction with membrane‐associated receptor proteins in animals and plants. eATP regulates plant growth, development, and responses to biotic and abiotic stresses. Its accumulation in the apoplast induces ROS production and cytoplasmic calcium increase mediating a defense response to invading microbes. We show here that perception of extracellular nucleotides, such as eATP, is important in plant–fungus interactions and that during colonization by the beneficial root endophyte Serendipita indica eATP accumulates in the apoplast at early symbiotic stages. Using liquid chromatography–tandem mass spectrometry, and cytological and functional analysis, we show that S. indica secrets SiE5′NT, an enzymatically active ecto‐5′‐nucleotidase capable of hydrolyzing nucleotides in the apoplast. Arabidopsis thaliana lines producing extracellular SiE5′NT are significantly better colonized, have reduced eATP levels, and altered responses to biotic stresses, indicating that SiE5′NT functions as a compatibility factor. Our data suggest that extracellular bioactive nucleotides and their perception play an important role in fungus–root interactions and that fungal‐derived enzymes can modify apoplastic metabolites to promote fungal accommodation. Synopsis: The beneficial fungal root endophyte Serendipita indica alters extracellular nucleotide levels and plant responses to biotic stresses. Extracellular ATP accumulates in the plant apoplast during root colonization by S. indica at early symbiotic stages.Perception of extracellular nucleotides, such as eATP, is important in plant‐fungus interactions.S. indica secrets E5′NT, an enzymatically active ecto‐5′‐nucleotidase that can modify apoplastic metabolites and promotes fungal accommodation. The beneficial fungal root endophyte Serendipita indica alters extracellular nucleotide levels and plant responses to biotic stresses. [ABSTRACT FROM AUTHOR]