DNA methylation affects the structure and function of genomes generating stable epigenetic marks. Nevertheless, genomes can become demethylated under particular replicative or nonreplicative conditions. We have recently demonstrated that the genome of Arabidopsis thaliana plants displays chromatin decondensation and DNA hypomethylation upon the attack of Pseudomonas syringae pv. tomato (Pst). This demethylation response affects repetitive sequences and single copy genes and it occurs in the absence of DNA replication suggesting it is mediated by an active process involving enzymes. We here analyze the effect of Pst-induced DNA demethylation on basal transcriptional activities of repetitive sequences and single copy genes, identifying genomic regions increasing transcription under infection. We also evaluate if MBD4, a potential DNA glycosidase, affects the host epigenetic changes described above. We found that chromatin condensation is normal in naïve mbd4/mbd4 mutant plants and that these plants displayed abnormal chromatin decondensation in response to Pst. In addition, we observed that mbd4/mbd4 plants have reduced vegetative growth and enhanced resistance against Pst. These results indicate that Pst-induced DNA demethylation affects the transcripcional activity of the host genome and suggest that MBD4 may participate in the phenomena of Pst-induced chromatin decondensation.