Clonal strains of the dinoflagellate Gymnodinium nolleri Ellegaard and Moestrup were intercrossed to determine if cyst-related traits are genetically regulated and to clarify unknown aspects in the sexuality of this species. The objectives were to determine whether the parental identity influenced the physiological and morphological aspects of the cyst offspring, and to describe and compare nuclear development and cell division of encysting and non-encysting zygotes. Variables characteristic of each parental cross (difference in growth rates among parents, cyst production (CP), and genetic distance (GD) among parents assessed via an amplified fragment length analysis analysis) were studied to seek for possible relationships of the parental crosses with some characteristics of the cyst offspring (cyst size, length of dormancy period, germination success, and germling viability (V)). A principal component analysis using these variables showed three main results: (1) the dormancy period of cysts responded to a simple pattern of inheritance, (2) the larger the GD between parents, the smaller the CP, and progeny V, and (3) the size of cysts was influenced by both CP and the parental strain identity. A stable inheritance of the short dormancy period (14.6±5.5 days), dominant over medium (31.0±8.5 days) and long periods (52.7±9.2 days), was confirmed through two subsequent generations of cysts. The regulation of the sexual processes by a multiple loci system is discussed based on the pattern of inheritance of the dormancy period and the number of sexual recombination events recorded within cultures with self-CP capability. Fusion of the gamete nuclei happened 0–48 h after the total cytoplasmic fusion. The nucleus of the zygote was bilobed and had thick and distinct chromosomes. Similar processes of nuclear and cell division occurred in the non-encysting or encysting planozygote, and were characterized by the loss of the chromosomal structure, an apparent increase of the DNA content, and the formation of thinner chromosomes.