It is becoming increasingly clear that microbes existing in equilibrium with the host are critical for immune homeostasis. While our understanding of the interaction between microbiota, especially their metabolic products like short-chain fatty acids (SCFA), and immunity at barrier tissues is growing, much less is known about how microbiota influence the more distal, circulating immune compartment. To address this, we have analyzed the development of circulating and tissue resident CD8+ T cell memory in germ-free mice combining in vivo approaches, genome-wide gene expression studies, and tissue metabolomics analysis. Interestingly, we observed that only circulating, but not tissue-resident memory CD8+ T cells failed to develop from effector cells in the absence of microbiota. This specific loss of circulating memory CD8+ T cells could be reverted by colonizing germ-free mice. CD8+ T cells isolated from germ-free mice showed particular disturbances in their mitochondrial metabolisms in comparison to cells from SPF mice. In addition, our data show that effector CD8+ T cells, deficient in the SCFA receptors GPR41/43, have a similarly decreased capacity to convert into circulatory memory T cells. Furthermore, effector CD8+ T cells, treated with SCFA during their initial differentiation phase, have an enhanced ability to develop into memory-precursor effector cells. Together, these findings highlight a previously unappreciated functional link between microbiota and the metabolic requirements of effector CD8+ T cells as they convert into circulating memory cells.