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Glyceollin isomers I, II, and III are the major pathogen-elicited secondary metabolites (i.e. phytoalexins) of soybean (<i>Glycine max</i>) that, collectively with other 5-deoxyisoflavonoids, provide race-specific resistance to <i>Phytophthora sojae.</i> The NAC-family transcription factor (TF) GmNAC42-1 is an essential regulator of some but not all glyceollin biosynthesis genes, indicating other essential TF(s) of the glyceollin gene regulatory network remain to be identified. Here, we conducted comparative transcriptomics on soybean hairy roots of the variety Williams 82 and imbibing seeds of Harosoy 63 upon treatment with wall glucan elicitor from <i>P. sojae</i> and identified two homologous R2R3-type MYB TF genes, <i>GmMYB29A1</i> and <i>GmMYB29A2</i>, up-regulated during the times of peak glyceollin biosynthesis. Overexpression and RNA interference silencing of <i>GmMYB29A2</i> increased and decreased expression of <i>GmNAC42-1</i>, <i>GmMYB29A1</i>, and glyceollin biosynthesis genes and metabolites, respectively, in response to wall glucan elicitor. By contrast, overexpressing or silencing <i>GmMYB29A1</i> decreased glyceollin I accumulation with marginal or no effects on the expressions of glyceollin synthesis genes, suggesting a preferential role in promoting glyceollin turnover and/or competing biosynthetic pathways. GmMYB29A2 interacted with the promoters of two glyceollin I biosynthesis genes in vitro and in vivo. Silencing <i>GmMYB29A2</i> in Williams 82, a soybean variety that encodes the resistance gene <i>Rps1k</i>, rendered it compatible with race 1 <i>P. sojae</i>, whereas overexpressing <i>GmMYB29A2</i> rendered the susceptible Williams variety incompatible. Compatibility and incompatibility coincided with reduced and enhanced accumulations of glyceollin I but not other 5-deoxyisoflavonoids. Thus, <i>GmMYB29A2</i> is essential for accumulation of glyceollin I and expression of <i>Phytophthora</i> resistance.