DNA methylation is an important heritable landmark conferring epigenetic changes in hybrids and has fascinated biologists and plant-breeders over the years. Although epigenetic changes have been documented in rice and maize hybrids, such investigations have not been reported in pigeonpea. Here, we report genome-wide methylation profiles of pigeonpea sterile and fertile inbred lines and their fertile F1 hybrid at single base resolution. We found that pigeonpea genome is relatively enriched in CG methylation. Identification of differentially methylated regions (DMRs) in the sterile and fertile parent revealed remarkable differences between their methylation patterns. Investigation of methylation status of parental DMRs in hybrid revealed non-additive methylation patterns resulting from trans-chromosomal methylation and trans-chromosomal demethylation events. Furthermore, we discovered several DMRs negatively associated with gene expression in the hybrid and fertile parent. Interestingly, many of those DMRs belonged to transposable elements and genes encoding pentatricopeptide repeats associated proteins, which may mediate a role in modulating the genes impacting pollen fertility. Overall, our findings provide an understanding of two parental epigenomes interacting to give rise to an altered methylome in pigeonpea hybrids, from genome-wide point of view.