A diploid-like pairing system prevents meiotic irregularities and improves the efficiency of gamete production in allopolyploid species. While the nature of the system is known in some polyploid crops including wheat, little is known about the control of chromosome pairing in polyploid fescues (Festuca spp.). In this work we studied chromosome pairing in allohexaploid F. arundinacea, its progenitors F. pratensis and F. glaucescens, and two intergeneric hybrids Lolium multiflorum (2x) ×F. arundinacea (6x) and L. multiflorum (4x) ×F. glaucescens(4x). The use of genomic in situ hybridization (GISH) permitted the analysis of homoeologous chromosome pairing and recombination of different genomes involved. We detected a diploid-like pairing system in polyploid fescues F. arundinacea and F. glaucescens, the latter being one of the progenitors of F. arundinacea. The pairing control system was absent in the second progenitor F. pratensis. Detailed analysis of intergeneric hybrids confirmed the presumed haploinsufficiency of the fescue system, which resulted in homoeologous pairing between all component genomes. This indicates that introgression of any specific chromosome segment from one genome to another is possible in all genome combinations. Our results not only contribute to the quest to discover the nature of the system controlling chromosome pairing in polyploid fescues, but may also have serious implications for design of hybrid breeding schemes in forage grasses.