The family of apicomplexa-specific proteins with DNA binding AP2 domains (ApiAP2s) includes sequence-specific transcription factors that are key regulators of development in malaria parasites. However, functions for the majority of ApiAP2 genes remain unknown. Here, a systematic knockout screen in Plasmodium berghei identifies ten ApiAP2 genes essential for mosquito transmission, of which four are critical for the formation of infectious ookinetes and three for sporogony. We describe unexpected non-essential functions for AP2-O and AP2-SP proteins in blood stages and identify AP2-G2 as a universal repressor active in both, asexual and sexual stages. Comparative transcriptomics across mutants and developmental stages reveals clusters of co-regulated genes with shared cis elements in their promoters, whose expression can be controlled positively or negatively by different ApiAP2 gene deletions. We propose that stage-specific interactions between ApiAP2 proteins on partly overlapping sets of target genes generate the complex transcriptional network that controls the Plasmodium life cycle.