The intracellular function of myosin motors requires a number of adaptor molecules, which control cargo attachment, but also fine-tune motor activity in time and space. These motor-adaptor-cargo interactions are often weak, transient or highly regulated. To overcome these problems we use a proximity labelling-based proteomics strategy (BioID) to map the interactome of the unique minus end-directed actin motor MYO6. Our analysis identified several distinct MYO6-adaptor modules including two complexes containing RHO GEFs which we screened using further BioID baits (LRCH3, DOCK7, GIPC1 and ARHGEF12). These complexes emphasise the multifunctionality of MYO6 provides the first in vivo interactome of a myosin motor protein, highlighting the power of this approach in uncovering dynamic and functionally diverse myosin motor complexes.