The plant cell wall is an actively reorganized network during plant growth and triggered immunity in response to biotic stress. While the molecular mechanisms managing perception, recognition, and signal transduction in response to pathogens are well studied in the context of damaging intruders, the current understanding of plant cell wall rebuilding and active defense strategies in response to plant virus infections remains poorly characterized. Pectins can act as major elements of the primary cell wall and are dynamic compounds in response to pathogens. Homogalacturonans (HGs), a main component of pectins, have been postulated as defensive molecules in plant–pathogen interactions and linked to resistance responses. This research focused on examining the regulation of selected pectin metabolism components in susceptible (rbohD-, Col-0-TuMV) and resistance (rbohF-, rbohD/F–TuMV) reactions. Regardless of the interaction type, ultrastructural results indicated dynamic cell wall rebuilding. In the susceptible reaction promoted by RbohF, there was upregulation of AtPME3 (pectin methylesterase) but not AtPME17, confirmed by induction of PME3 protein deposition. Moreover, the highest PME activity along with a decrease in cell wall methylesters compared to resistance interactions in rbohD–TuMV were noticed. Consequently, the susceptible reaction of rbohD and Col-0 to TuMV was characterized by a significant domination of low/non-methylesterificated HGs. In contrast, cell wall changes during the resistance response of rbohF and rbohD/F to TuMV were associated with dynamic induction of AtPMEI2, AtPMEI3, AtGAUT1, and AtGAUT7 genes, confirmed by significant induction of PMEI2, PMEI3, and GAUT1 protein deposition. In both resistance reactions, a dynamic decrease in PME activity was documented, which was most intense in rbohD/F–TuMV. This decrease was accompanied by an increase in cell wall methylesters, indicating that the domination of highly methylesterificated HGs was associated with cell wall rebuilding in rbohF and rbohD/F defense responses to TuMV. These findings suggest that selected PME with PMEI enzymes have a diverse impact on the demethylesterification of HGs and metabolism as a result of rboh–TuMV interactions, and are important factors in regulating cell wall changes depending on the type of interaction, especially in resistance responses. Therefore, PMEI2 and PMEI3 could potentially be important signaling resistance factors in the rboh–TuMV pathosystem.