Hallmark features of adaptive CD4+ T-cells include differentiation into multiple effector T helper (Th) fates and subsequent emergence of memory states. Fate mapping, adoptive transfer and single-cell tracking approaches in mouse models of acute viral or bacterial infection suggest that memory CD4+ T cells develop directly from effector precursors. However, molecular pathways governing these developmental transitions remain undefined. Here we tested the hypothesis that CD4+ Th cells directly convert into memory CD4+ T cells during malaria in vivo, and in doing so defined underlying transcriptomic processes. Tracking endogenous TCR sequences via TraCeR analysis firstly confirmed that sibling clones populated both Th1 and Tfh fates. Instead of transitioning through a memory precursor population, two memory cell lineages were detected to originate directly from either T helper 1 (Th1) or follicular T helper (Tfh) effector cells. Memory development in both lineages were characterized over three weeks by a progressive 50% reduction in the numbers of genes expressed, as well as partial transcriptomic convergence towards memory. Low-level persisting infection in this model diverted but did not block memory development, which was associated instead with onset of partial exhaustion. We inferred within the Th1-lineage a linear transition from Th1 via Type 1 regulatory T (Tr1) to effector memory T (TEM) cells, with TEM cells poised for Th1 re-call. In contrast, the Tfh-lineage exhibited a modest Th1-signature throughout, no evidence of Tr1 development, and lineage-specific co-expression of central memory T (TCM) markers. A subset of memory-associated genes was also defined, including transcription factors Id2 and Maf, whose expression increased progressively against a background of transcriptomic quiescence. Thus, by examining transcriptional dynamics using scRNA-seq, we describe the molecular pathways taken by effector CD4+ T cells towards memory.