Arbuscular mycorrhizal fungi (AMF), the mutualistic symbionts with most crops, constitute a research system of human-associated fungi whose relative simplicity and synchrony are conducive to experimental ecology. However, little is known about the shifts in adaptive strategies of sorghum associated AMFs where strong AMF succession replaces initially ruderal species with competitive ones and where the strongest plant response to drought is to manage these AMF. First, we hypothesize that, when irrigation is stopped to mimic drought, competitive AMF species should be replaced by AMF species tolerant to drought stress. We then, for the first time, correlate AMF abundance and host plant transcription to test two novel hypotheses about the mechanisms behind the shift from ruderal to competitive AMF. Surprisingly, despite imposing drought stress, we found no stress tolerant AMF. Remarkably, we found strong and differential correlation between the successional shift from ruderal to competitive AMF and sorghum genes whose products (i) produce and release strigolactone signals, (ii) perceive mycorrhizal-lipochitinoligosaccharide (Myc-LCO) signals, (iii) provide plant lipid and sugar to AMF and, (iv) import minerals and water provided by AMF. These novel insights into host gene expression and succession of AMF show adaptive strategies evolved by AMF and their hosts and provide a rationale for selecting AMF to reduce inputs and maximize yield in commercial agriculture. Future research opportunities include testing the specifics and generality of our hypotheses by employing genetically modified host plants, and exploring additional genes underlying the adaptive strategies in natural succession.