A variety of plausible mechanisms for methane hydroxylation in methane monooxygenases (MMO) have been tested by high-level quantum chemical methods on model systems with simple ligands chosen on the basis of the MMO crystal structure and the available biophysical data. One pathway survives the present level of tests in having intermediates with plausible energies and structures and a low-energy transition state for C-H abstraction. In this proposed pathway, the Fe-2(II,II) dinuclear iron site of the reduced form of MMO reacts with O-2 to give two different Fe-2(III,III) peroxo species and, after O-O bond cleavage, an Fe-2(IV,IV) bis-mu-oxo species probably directly analogous to "compound Q" of MMO. As a result of the large Jahn-Teller distortions in the d(4) bis-mu-oxo species, the Fe-O-Fe bridges are highly asymmetric, allowing the system to open up easily to a key Fe-III-O-Fe-V=O intermediate that is shown to be capable of reacting with methane via a low-energy transition state. This intermediate is shown to be better regarded as having the structure Fe-III-O-Fe-IV-O-., with radical character at the terminal oxo group. After H atom abstraction from methane, the methyl radical recombines very rapidly with the Fe center via a weak Fe-CH3 bond. With the loss of CH3OH, an Fe-III-O-Fe-III dimer is formed that requires reduction to form the Fe-2(II,II) starting species. In addition to the work on the dinuclear species, results on a number of relevant mononuclear Fe(III) and Fe(IV) species are also reported.