BackgroundThe function of DNA methyltransferase genes of insects is a puzzle, because an association between gene expression and methylation is not universal for insects. If the genes normally involved in cytosine methylation are not influencing gene expression, what might be their role? We previously demonstrated that gametogenesis ofOncopeltus fasciatusis interrupted at meiosis following knockdown ofDNA methyltransferase 1(Dnmt1) and this is unrelated to changes in levels of cytosine methylation. Here, using transcriptomics, we tested the hypothesis thatDmnt1is a part of the meiotic gene pathway. Testes, which almost exclusively contain gametes at varying stages of development, were sampled at 7 days and 14 days following knockdown ofDmnt1using RNAi.ResultsUsing microscopy, we found actively dividing spermatocysts were reduced at both timepoints. However, as with other studies, we sawDnmt1knockdown resulted in condensed nuclei after mitosis–meiosis transition, and then cellular arrest. We found limited support for a functional role forDnmt1in our predicted cell cycle and meiotic pathways. An examination of a priori Gene Ontology terms showed no enrichment for meiosis. We then used the full data set to reveal further candidate pathways influenced byDnmt1for further hypotheses. Very few genes were differentially expressed at 7 days, but nearly half of all transcribed genes were differentially expressed at 14 days. We found no strong candidate pathways for howDnmt1knockdown was achieving its effect through Gene Ontology term overrepresentation analysis.ConclusionsWe, therefore, suggest thatDmnt1plays a role in chromosome dynamics based on our observations of condensed nuclei and cellular arrest with no specific molecular pathways disrupted.Supplementary InformationThe online version contains supplementary material available at 10.1186/s13072-023-00496-5.