BackgroundFamilial breast cancer is in most cases unexplained due to the lack of identifiable pathogenic variants in theBRCA1andBRCA2genes. The somatic mutational landscape and in particular the extent of BRCA-like tumour features (BRCAness) in these familial breast cancers where germlineBRCA1orBRCA2mutations have not been identified is to a large extent unknown.MethodsWe performed whole-genome sequencing on matched tumour and normal samples from high-risk non-BRCA1/BRCA2breast cancer families to understand the germline and somatic mutational landscape and mutational signatures. We measured BRCAness using HRDetect. As a comparator, we also analysed samples fromBRCA1andBRCA2germline mutation carriers.ResultsWe noted for non-BRCA1/BRCA2tumours, only a small proportion displayed high HRDetect scores and were characterized by concomitant promoter hypermethylation or in one case a RAD51D splice variant previously reported as having unknown significance to potentially explain their BRCAness. Another small proportion showed no features of BRCAness but had mutationally active tumours. The remaining tumours lacked features of BRCAness and were mutationally quiescent.ConclusionsA limited fraction of high-risk familial non-BRCA1/BRCA2breast cancer patients is expected to benefit from treatment strategies against homologue repair deficient cancer cells.Supplementary InformationThe online version contains supplementary material available at 10.1186/s13058-023-01655-y.