The interplay between genetic and epigenetic factors plays a central role in mammalian embryo production strategies that superimpose ex vivo or in vivo manipulations upon strain background characteristics. In this study, we examined the relationship between genetic background and the phenotypic properties of mouse metaphase-II (M-II) oocytes that were matured under in vivo (IVO) or in vitro conditions, either in a basal (IVM) or a supplemented (IVM +) medium. Differences existed amongst inbred (C57BL/6), outbred (CF-1, Black Swiss, NU/NU) and hybrid lines (B6D2F1) induced to superovulate with regard to cytoplasmic microtubule organizing center (MTOC) number but not spindle size or shape, except for larger and asymmetrical spindles in Black Swiss oocytes. When oocytes were matured in culture, meiotic spindle and cytoplasmic phenotypic properties of M-II oocytes were affected relative to in vivo conditions and between strains. Specifically, measures of meiotic spindle size, shape, polar pericentrin distribution and cytoplasmic MTOC number all revealed characteristic variations. Interestingly, the overall reduction in cytoplasmic MTOC number noted upon IVM was concomitant with an overall increase in spindle and polar body size. Maturation under IVM + conditions resulted in a further decrease in cytoplasmic MTOC number, but spindle and polar body characteristics were intermediate between IVO and IVM. How these oocyte phenotypic properties of maternal origin may be linked to predictive assessments of fecundity remains to be established. © 2005 Society for Reproduction and Fertility.