Parasitic worms (helminths) survive in their animal hosts by inactivating innate detection systems and subsequently manipulating the immune response to prevent their expulsion. Understanding how these pathogens manipulate host immune responses will inform the development of novel strategies for infection control. It is now broadly acknowledged that non-coding RNA (ncRNA) play a critical role in the regulation of innate immune response. We propose that by releasing miRNAs for uptake by host immune cells, helminths hijack the host miRNA machinery to regulate the expression of host gene targets to control the immune response, thus allowing the parasite to establish chronic infections. Mice were infected with the liver fluke Fasciola hepatica, and macrophages were isolated 6h, 18h and 5 days post-infection and subjected to miRNA and total RNA sequencing. This revealed an enrichment of several parasitic-derived miRNAs (fhe-miR-277b-3p, fhe-miR-71a-5p, fhe-miR-125b-5p, fhe-miR-125a-5p) within macrophages at 6h and 18h after infection. This regulation appears to be temporal as they were not present at day 5 post-infection. Target prediction analysis, combined with RNA sequencing, indicated that these Fasciola miRNAs regulated host genes associated with innate immune regulation (predominantly Hif1a, Nod1, Nlrp6 and P2rx7), specifically to suppress the development of pro-inflammatory, host protective, M1 macrophages. At the same time, there was a distinct shift in host ncRNA (miRNA and long non-coding RNA) expression. Target prediction analysis suggested that these host ncRNAs target a different cohort of genes (predominantly ADAR1 and IGF1) to the parasite miRNAs, the altered expression of which is associated with the induction of pro-inflammatory M1 macrophages. This level of characterisation of the ncRNA landscape in macrophages during helminth infection is highly novel and provides unique insight into the molecular impact a parasite induces on a host and reveals a competing regulation of immune response between the host and parasite.