Alternative splicing is poorly characterised in eukaryotes outside animals and yeast, but protists with small, densely-packed genomes and compact gene structure are particularly well suited to characterising whole-genome regulation of splicing. We have studied the protist parasites Plasmodium and Toxoplasma, causative agents of malaria and toxoplasmosis, to characterise basic features of alternative splicing, and to compare these divergent parasites to complex multicellular eukaryotes. Because these parasites have much smaller genomes than animals, we are able to assemble whole transcriptomes using single MinION flow cells by applying direct nanopore sequencing of RNA. We find extensive alternative splicing in these transcriptomes, and show that splicing patterns change between life stages of these parasites. However, the pattern of splicing departs from that seen in better characterised eukaryotes, with intron retention being widespread. We find clear biological roles for a handful of alternative isoforms, but most alternative splicing events produce apparently nonproductive isoforms. To interrogate the role of alternative splicing in these parasites, we have comprehensively disrupted the family of Serine/Arginine (SR) splice regulators and the SR kinases in Plasmodium and Toxoplasma and characterised transcriptomes from these disrupted lines. We show that different SR proteins are required for regulation of splicing at different life stages, and that SR proteins and SR kinases govern overlapping but distinct repertoires of transcripts. Our data show a complex system of splice regulation in these transcriptomes that is required for normal growth and differentiation. We also reveal an abundance of alternative splicing that produces nonproductive transcripts, which are apparently tolerated despite their frequency.