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ABSTRACT Background and Aims Hybrid seed failure (HSF) is a common reproductive barrier in flowering plants, but how divergence in so-called ‘effective ploidy’ translates into genome-wide allelic imbalance in hybrid endosperm remains unresolved. Using wild tomatoes ( Solanum sect. Lycopersicon ) as our model system, we test whether parent-of-origin expression shifts in hybrids are consistent with simple dosage effects or instead reflect lineage-specific trans regulation. Methods Using reciprocal interspecific crosses, we quantified parent-of-origin (allele-specific) expression in developing endosperm and analyzed patterns of differential parent-of-origin expression (DPE) across cross contexts. Guided by strong patterns in parental expression, we further classified DPE genes into four functional classes defined by their relationship to Solanum peruvianum ( Per ). This exercise captured distinct modes of trans -allelic regulation and guided functional interpretation. Key Results Parental expression proportions are strongly asymmetric in hybrids, with the most pronounced and repeatable shifts occurring in crosses involving Per . These shifts recur across reciprocal contexts and include elevated maternal proportions even in crosses phenotypically classified as paternal-excess-like, arguing against a dosage-only model. Instead, we observed cross-consistent, coordinated DPE patterns corresponding to trans -acting dominance associated with Per . Functional enrichment of Per -associated DPE highlights chromatin regulation, including DNA methylation/RdDM- and chromatin remodeling-related factors, and Polycomb-linked regulators, implicating disruption of chromatin-based repression in hybrid endosperm. Concurrently, Per -associated activation of auxin- and cell-cycle regulatory pathways in non- Per alleles suggests mis-timed hormone-dependent developmental transitions that can destabilize proliferation–cellularization programs. Conclusions Our findings support a model of trans -allelic epigenetic dominance in which Per -associated regulatory inputs reshape allelic expression landscapes in hybrid endosperm largely independent of parental origin. This provides a mechanistic link between effective ploidy divergence, genome-wide transcriptional imbalance, and HSF, and motivates reciprocal hybrid studies that integrate expression with chromatin-state and accessibility profiling.