Fancy breeds of Japanese indigenous chicken display extensive morphological diversity, particularly in tail feathers. Although marked differences in tail and bone traits have been reported between Tosa‐jidori (wild type) and Minohikichabo (rich type) breeds, little is known about the pattern of genetic inheritance in cross experiments. Therefore, this study aimed to investigate the strain and sex effects, and inheritance patterns, in the morphometric variation of pygostyle bones among Tosa‐jidori, Minohikichabo, and their F1 hybrids. Five morphological traits, angle of the apex of the pygostyle, pygostyle length, margo cranialis length, tail feather number, and body weight, were evaluated at the adult stage. A significant strain difference was detected in all traits, whereas significant sex differences were observed in only three traits, but not in the angle of the apex of the pygostyle and tail feather number. In F1 hybrids, the angle of the apex of the pygostyle was significantly different to that of Tosa‐jidori but not that of Minohikichabo, whereas the pygostyle length and tail number of F1 hybrids were significantly different from those of Minohikichabo but not those of Tosa‐jidori. A significant heterosis effect was found in the margo cranialis length and body weight. All five traits showed nonadditive inheritance patterns but varied in each trait between partial dominance (angle of the apex of pygostyle), full dominance (pygostyle length and tail feather number), and over‐dominance (margo cranialis length and body weight). Interestingly, different patterns of genetic inheritance in the F1 hybrid were observed at different locations, even within the same pygostyle bone. Using the Japanese indigenous chicken model, these results provide a substantial step toward understanding the genetic architecture of morphology in chickens.