Using high resolution quantitative mass spectrometry we have explored how immune activation and the metabolic checkpoint kinase mTORC1 (mammalian target of rapamycin complex 1) regulate the proteome of B lymphocytes. Triggering the B cell receptor, CD40 and the IL-4 receptor induced considerable re-modelling of the B cell protein landscape, with a 5-fold increase in total cellular protein mass within 24 hours of activation. Analysis of copy numbers per cell of >7,500 proteins revealed the metabolic machinery that supports B cell activation and identified the nutrient and amino acid transporters that fuel B cell biosynthetic capacity. We reveal that mTORC1 controls activation-induced cell growth and B cell proteome remodelling. We show that mTORC1 is critical for the expression of transcription factors that regulate B cell differentiation and metabolism including MYC. mTORC1 activity is required for B cells to sustain MYC expression during activation and inhibiting mTORC1 impairs the expression of nutrient and amino acid transporters that fuel B cell protein production. This work provides a detailed map of naïve and immune activated B cell proteomes and a greater understanding of the cellular machinery that direct B cell phenotypes. This work also provides new insights into the role of mTORC1 and MYC in regulating activation induced proteome remodelling and protein production in B cells.