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Chromosome segregation errors in mammalian oocyte meiosis lead to developmentally compromised aneuploid embryos and become more common with advancing maternal age. Known contributors include age‐related chromosome cohesion loss and spindle assembly checkpoint (SAC) fallibility in meiosis‐I. But how effective the SAC is in meiosis‐II and how this might contribute to age‐related aneuploidy is unknown. Here, we developed genetic and pharmacological approaches to directly address the function of the SAC in meiosis‐II. We show that the SAC is insensitive in meiosis‐II oocytes and that as a result misaligned chromosomes are randomly segregated. Whilst SAC ineffectiveness in meiosis‐II is not age‐related, it becomes most prejudicial in oocytes from older females because chromosomes that prematurely separate by age‐related cohesion loss become misaligned in meiosis‐II. We show that in …