One of the most intriguing outcomes of hybridization is the emergence of asexual hybrids, where canonical gametogenesis is altered, leading to clonal or hemiclonal genome propagation. However, maintaining these lineages is challenging due to frequent irregularities in gamete formation. These irregularities increase the diversity of gametogenic pathways, though their triggers and outcomes remain unknown. We studied these processes in water frog hybrids from the Pelophylax esculentus complex, which reproduce asexually via hybridogenesis. During this process, P. esculentus hybrids usually produce gametes with a genome from either P. ridibundus or P. lessonae. Using fluorescent in situ hybridization with probes to species-specific satellite repeats, we identified genome composition in spermatocytes and spermatids from 47 hybrid males collected from four localities in Eastern Ukraine. Some males exclusively eliminated either the P. ridibundus or P. lessonae genome, suggesting selection before meiosis. Other males transmitted gametes with both genomes simultaneously, indicating elimination of one genome from different gonocyte populations. Such variability in gametogenic pathways among males from different localities implied independent hybrid origins. Additionally, abnormal pairing between P. ridibundus and P. lessonae chromosomes during meiosis indicated an inability to eliminate and endoreplicate genomes of parental species. By comparative genome hybridization, we for the first time identified intensive genome rearrangements between ridibundus and lessonae chromosomes and unstained chromosomal parts suggesting the introgression of different species genome in such hybrids. These genomic rearrangements and introgressions affect hybridogenetic reproduction, causing aneuploidy in gametes.