Trypanosomes are global blood parasites that infect a wide range of vertebrate hosts. Several species of Trypanosoma cause disease in humans and domesticated animals, and the majority are transmitted between hosts by haematophagous invertebrate vectors. Ticks have long been speculated as vectors for Australian trypanosomes. Recent studies using advanced molecular techniques have refocused attention on these arthropods, and whilst they have renewed discussions about Trypanosoma species and their vectors, these reports have simultaneously led to premature conclusions concerning the role of ticks as vectors. Here the controversy surrounding ticks as trypanosome vectors is discussed. We highlight the unanswered questions concerning the role played by ticks in trypanosome transmission and suggest future approaches to resolving these key knowledge gaps.