Leaf curl disease of tomato caused by Tomato Leaf Curl New Delhi Virus (ToLCNDV) inflicts huge economical loss. Disease symptoms resemble leaf developmental defects including abnormal vein architecture. Leaf vein patterning related TORNADO1 gene’s ( SlTRN1 ) transcript level is augmented in virus-infected leaves. To elucidate the molecular mechanism of the upregulation of SlTRN1 in vivo we have deployed SlTRN1 promoter-reporter transgenic tomato plants and investigated the gene’s dynamic expression pattern in leaf growth stages and infection. Expression of the gene was delimited in the vascular tissues and oppressed in growing leaves. Methylation-sensitive PCR analyses confirmed the accumulation of CHH methylation at multiple locations in the SlTRN1 promoter in older leaves. However, ToLCNDV infection reverses the methylation status and restores expression level in the leaf vascular bundle. The virus dampens the level of key maintenance and de novo DNA methyltransferases SlDRM5 , SlMET1 , SlCMT2 with concomitant augmentation of two DNA demethylases, SlDML1 and SlDML2 levels in SlTRN1 promoter-reporter transgenics. Transient overexpression of SlDML2 mimics the virus-induced hypomethylation state of the SlTRN1 promoter in mature leaves. Further, in line with the previous studies, we confirm the crucial role of viral suppressors of RNA silencing AC1 and AC4 proteins in promoting DNA demethylation and directing it to reinstate activated transcription of SlTRN1 in silenced tissues for possible modification of leaf venation architecture, leaf curling and easy vector acquisition of viral particles.