We revisit the moduli space approximation to the quantum mechanics of monopoles in N=4 supersymmetric Yang-Mills-Higgs theory with maximal symmetry breaking. Starting with the observation that the set of fermionic zero-modes in N=4 supersymmetric Yang-Mills-Higgs theory can be viewed as two copies of the set of fermionic zero-modes in the N=2 version, we build a model to describe the quantum mechanics of N=4 supersymmetric monopoles, based on our previous paper (de Vries and Schroers, 2009)  on the N=2 case, in which this doubling of fermionic zero-modes is manifest throughout. Our final picture extends the familiar result that quantum states are described by differential forms on the moduli space and that the Hamiltonian operator is the Laplacian acting on forms. In particular, we derive a general expression for the total angular momentum operator on the moduli space which differs from the naive candidate by the adjoint action of the complex structures. We also express all the supercharges in terms of (twisted) Dolbeault operators and illustrate our results by discussing, in some detail, the N=4 supersymmetric quantum dynamics of monopoles in a theory with gauge group SU(3) broken to U(1)×U(1). © 2010 Elsevier B.V.