Malaria parasites (Plasmodium spp.) include some of the world's most widespread and virulent pathogens, infecting a wide array of vertebrates. Our knowledge of the molecular mechanisms these parasites use to invade and exploit hosts other than mice and primates is, however, extremely limited. How do Plasmodium adapt to individual hosts and to the immune response of hosts throughout an infection? To better understand parasite plasticity, and identify genes that are conserved across the phylogeny, it is imperative that we characterize transcriptome-wide gene expression from non-model malaria parasites in multiple host individuals. Here, we used high-throughput Illumina RNA-sequencing on blood from wild-caught Eurasian siskins experimentally infected with a clonal strain of the avian malaria parasite, Plasmodium ashfordi (lineage GRW2). By using a multi-step approach to filter out all host transcripts, we successfully assembled the blood-stage transcriptome of P. ashfordi. A total of 11 954 expressed parasite transcripts were identified, and 7 860 were annotated with protein information. We further quantified gene expression levels of all parasite transcripts across three hosts during two infection stages - peak and decreasing parasitemia. Interestingly, parasites from the same host during different infection stages displayed remarkably similar expression profiles, but show large differences across hosts. This indicates that P. ashfordi adjusts its gene expression to specific host individuals, but contrary to expectation does not markedly change expression across different stages of infection. Finally, we examined genome-wide sequence similarity between P. ashfordi and other apicomplexan species, and searched for candidate genes involved in red blood cell invasion. The majority of transcripts were most similar to the human parasite Plasmodium falciparum, and a large number of invasion genes were discovered, suggesting conserved red blood cell invasion strategies between mammalian and avian Plasmodium spp. The transcriptome of P. ashfordi and its host-specific gene expression over two infection stages advances our understanding of Plasmodium plasticity and will become a valuable resource as it allows for further studies analyzing gene evolution and comparisons of parasite gene expression.