Multi-omics provide a novel opportunity to study the interactions of fungi from different functional guilds in host plants in field conditions. We address the entangled responses of pathogenic and endophytic fungi associated with sorghum when droughted through assembly of the most abundant fungal, endophyte genome from rhizospheric metagenomic sequence followed by comparison of its metatranscriptome with the host plant metabolome and transcriptome. The rise of endophyte abundance in drought co-occurs with a rise in fungal membrane dynamics and plant metabolites, led by ethanolamine, a key phospholipid membrane component. The negative association between endophyte and plant pathogenic fungi associates with a rise in expression of the endophyte’s biosynthetic gene clusters coding for secondary compounds. Among them is a siderophore suggesting iron as the resource limiting abundance of both endophyte and pathogens. Surprisingly, we found no evidence that reduction in relative abundance of pathogenic fungal is associated with plant hormones or immunity.