Single-celled Plasmodium spp. malaria parasites are responsible for more than 2 million cases of severe disease annually. These parasites have distinct lifecycle stages spanning multiple hosts and so strict regulation of gene and protein expression is critical for stage transition and parasite survival. Despite this, the molecular mechanisms malaria parasites utilise to regulate gene and protein expression remain poorly understood. The putative malaria parasite DNA/RNA binding protein Alba4 (Acetylation lowers binding affinity) is implicated in key parasite regulatory processes including post-transcriptional regulation and stage differentiation. Here, we utilised gene-editing and complementary proteomics approaches to understand the protein interaction network and function of PfAlba4 in late blood stage Plasmodium falciparum parasites. Using an established episomally expressed miniTurbo-BioID system, proteins in close proximity to PfAlba4 were biotin labelled, isolated and then identified with mass spectrometry, leading to the identification of >50 high-confidence potential protein interactors of PfAlba4 with ~23% of these being of unknown function. As secondary confirmation of the proximity interactome for PfAlba4, we applied and validated a custom built Split-TurboID system designed to minimise cellular-toxicity from the biotinylating enzyme, which demonstrated >23% overlap in high confidence potential PfAlba4 interactors. A gene-edited parasite line was then generated for one protein identified in both BioID datasets (PF3D7_0706500) and utilised for co-immunoprecipitation experiments that supported a direct interaction of PF3D7_0706500 with PfAlba4. Gene ontology and K means clustering analysis using the string database revealed an enrichment of proteins involved in the negative regulation of translation – including the CCR4-NOT complex, Eukaryotic translation initiation factor 4F complex, and proteins associated with nuclear-transcribed mRNA catabolism/nonsense-mediated decay – for both PfAlba4 and its putative interacting partner PF3D7_0706500. Together, these data suggest PfAlba4 is a key regulator of mRNA translation and decay during malaria parasite blood stage development. The gene-edited lines and high-quality preliminary interactome developed in this study will enable characterisation of PfAlba4’s essential cell regulatory function and potentially identify additional key regulatory proteins that could be targets for antimalarial development.