Abstract Specific metabolic programs are activated by immune cells to fulfil their functional roles, which include adaptations to their microenvironment. B1 B cells are tissue-resident, innate-like B cells. They have many distinct properties, such as the capacity to self-renew and the ability to rapidly respond to a limited repertoire of epitopes. The metabolic pathways that support these functions are unknown. We show that B1 B cells are bioenergetically more active than B2 B cells, with higher rates of glycolysis and oxidative phosphorylation, and depend on glycolysis. They acquire exogenous fatty acids, and store lipids in droplet form. Autophagy is differentially activated in B1a B cells, and deletion of the autophagy gene Atg7 leads to a selective loss of B1a B cells due to a failure of self-renewal. Autophagy-deficient B1a B cells downregulate critical metabolic genes and accumulate dysfunctional mitochondria. B1 B cells therefore, have evolved a distinct metabolism adapted to their residence and specific functional properties.