Environmental adaptation of organisms relies on fast perception and response to external signals, which lead to developmental changes. Plant cell growth is strongly dependent on cell wall remodeling. However, little is known about cell wall‐related sensing of biotic stimuli and the downstream mechanisms that coordinate growth and defense responses. We generated genetically encoded pH sensors to determine absolute pH changes across the plasma membrane in response to biotic stress. A rapid apoplastic acidification by phosphorylation‐based proton pump activation in response to the fungus Fusarium oxysporum immediately reduced cellulose synthesis and cell growth and, furthermore, had a direct influence on the pathogenicity of the fungus. In addition, pH seems to influence cellulose structure. All these effects were dependent on the COMPANION OF CELLULOSE SYNTHASE proteins that are thus at the nexus of plant growth and defense. Hence, our discoveries show a remarkable connection between plant biomass production, immunity, and pH control, and advance our ability to investigate the plant growth‐defense balance. Synopsis Plant pathogens, including the fungus Fusarium oxysporum, modulate plant apoplastic pH to facilitate infection. Here, F. oxysporum infection is shown to induce a rapid plant response via pH‐dependent modulation of cell wall structure and root growth, which controls fungal pathogenesis. F. oxysporum infection triggers reduction of cellulose synthesis and inhibition of root growth. Genetically encoded pH sensors show rapid plant apoplastic acidification upon F. oxysporum contact due to proton pump activation at the plasma membrane. Infection‐induced pH changes influence plant cellulose synthesis, growth, and fungal virulence. The COMPANION OF CELLULOSE SYNTHASE proteins CC1 and CC2 suppress proton pump activity. cc1cc2 mutant plants are less sensitive to fungal infection. Induction of apoplast acidification and modification of cell wall properties to control fungal infection are regulated by the COMPANION OF CELLULOSE SYNTHASE proteins at the nexus of plant growth and defense.