Blowfly (Diptera: Calliphoridae) exhibit diverse feeding strategies, with most species developing on decomposing organic matter. However, parasitism has evolved within the family, and some species convergently gained the ability to explore the tissues of living vertebrate hosts, which imposes critical veterinary, medical, and agricultural issues worldwide. It is yet unknown how this phenotype has evolved and whether it is determined by the same genetic architecture in different species or not. To address these questions, we evaluated key behavioural phenotypes in species with contrasting feeding habits, focusing on female oviposition preferences and larval survival on distinct diets, both critical aspects of their life cycles. These assays allowed us to propose hypotheses of how oviposition and larval behaviours contribute to feeding habits displayed in nature for parasitic and saprophagous species. Additionally, a transcriptome-wide analysis revealed genes and functional pathways potentially linked to parasitic behaviour by comparing gene expression profiles and coding sequence evolution. In the genetic analysis, we identified genes with important functions related to the measured behaviours, revealing that distinct genes may underlie each independent case of parasitism evolution, suggesting a non-parallel evolutionary pathway for this convergent trait.