Lima1 is an extensively studied prognostic marker of malignancy and is also considered to be a tumour suppressor, but its role in a developmental context of non-transformed cells is poorly understood. Here, we characterised the expression pattern and examined the function of Lima1 in mouse embryos and pluripotent stem cell lines. We found that Lima1 expression is controlled by the naïve pluripotency circuit and is required for the suppression of membrane blebbing. Moreover, Lima1 is essential for proper mitochondrial energetics, which is crucial for the growth of solid tumours. Forcing Lima1 expression enabled human pluripotent stem cells to be incorporated into murine pre-implantation embryos, trespassing the interspecies engraftment barrier. Thus, Lima1 is a key effector molecule that mediates the pluripotency control of membrane dynamics and cellular metabolism.