Clostridiodes difficile is a major cause of hospital-associated infection and recurrent antibiotic-associated diarrhoea, yet phage-based strategies remain understudied. Therapeutic development has been slow due to a lack of naturally occurring strictly lytic phages, high strain-specificity and incomplete understanding of their infection mechanisms. This knowledge gap hinders our understanding of phage-host interactions, and while previous research has provided some insights into structure and function, further investigation is necessary. To address these challenges, we established a versatile phage engineering platform that enables precise genetic modification of two C. difficile bacteriophages. Using this system, we introduced a protein tag to facilitate cargo delivery and are developing aptamer-based tools for live imaging of infection dynamics. We also engineered the phage tail needle to understand its role in host recognition and final infection, and created a plaque-independent method for quantifying phage titres. High-resolution cryo-EM reconstructions provided complementary structural insights into tail architecture and contraction, helping to link molecular structure with infection mechanism. Together, these complementary genetic, biochemical, and structural approaches offer new mechanistic insights into C. difficile phage biology and open the way for the rational design of optimised therapeutic phages.