Pesticides are known to induce genome instability. Report on eukaryotes, including humans, mostly covers chromosomal aberrations and DNA strand breaks. Studies on the scoring of the rates of loci-specific somatic mutations such as point mutations (PM), somatic homologous recombination (SHR), frameshift mutation (FSM), and transpositions due to pesticides are mostly confined to prokaryotes using Ames test. Analogous eukaryotic model systems though are available for Drosophila, mouse and certain cell lines, reports using these are meagre possibly due to the lethality of commercially-used pesticide doses and/or difficulty in assessing large population. DNA replication/repair being highly conserved among the higher eukaryotes, we used the plant-based system of Arabidopsis thaliana to score various loci-specific mutations. This study revealed that the pesticides malathion, flubendiamide, chlorantraniliprole, and carbendazim + mancozeb combination not only increased the rates of loci-specific PM, SHR and FSM, and caused epimutations on selected DNA repair gene promoters, but also induced heritable transgenerational memory of certain alterations. While SHR rates were significantly high in the untreated progeny, FSM rates were high even in the grand progeny. Expression of 15 DNA repair genes analysed showed an increase under at least one of the pesticidal treatments. Out of 21 DNA repair gene promoters analysed, eight showed altered methylation. Of these, only MRE11A (homologous recombination pathway) promoter showed demethylation in the untreated progeny, due to all four pesticides. Malathion-induced demethylation was retained in the grand progeny also. Thus this work gauges the severity of various pesticides on inducing heritable mutations/epimutations in a non-target system.