Lymphatic filariasis (LF), caused by mosquito-borne filarial nematodes, is one of the most debilitating of the neglected tropical diseases. Great progress has been made in control programs based on mass drug administration, but sustaining the success requires a better understanding of parasite biology and host-parasite interactions. The purpose of the present study was to enhance our understanding of mosquito cellular immunity, filarial parasite development and the interaction of developing parasites with the mosquito host, using high-throughput transcriptomic approaches as a primary investigative tool. To this end, studies were designed to characterize transcripts enriched in Aedes aegypti hemocytes, the blood cells that mediate innate immune responses, including phagocytosis, melanization, and production of antimicrobial peptides. Genome-wide microarray analysis of genes that exhibit tissue specificity following immune challenge provided a detailed overview of the hemocyte molecular repertoire, likely involved in cell type specific functions that coordinate the actions of different infection responsive tissues. To better understand the parasite developmental processes required for the infectious cycle, research efforts were directed to comparatively analyze the different life stages of the filarial worm Brugia malayi. RNA-seq analysis revealed transitions in gene expression from eggs through larval stages to adults, including patterns of sex-biased or germline-enriched expression, potentially implicated in reproductive processes. Discrete transcriptional changes were observed during maturation of microfilariae and the third- to fourth-stage larval transition that are vital for infection in mosquito vectors and vertebrate hosts, respectively. Finally, experiments were conducted to investigate the in vivo transcriptome dynamics of B. malayi during its obligatory intracellular developmental phase in the mosquito. Integrative analysis of the host transcriptome in a dual RNA-seq approach revealed the temporal organization of transcriptional events in both the nematode and the host tissue. Parasite gene transcription dynamics exhibited a highly ordered developmental program consisting of a series of cyclical and state-transitioning temporal patterns, which was contextualized in relation to the concurrent dynamics of the host tissue transcriptome. These data provided new perspective and insight into filarial worm-mosquito interactions, which will lead to future systems-level studies to further our understanding of this symbiotic relationship responsible for the perpetuation of LF.