We investigate the nature of CO emission from z~6 quasars by combining non-LTE radiative transfer calculations with merger-driven models of z~6 quasar formation that arise naturally in LCDM cosmological simulations. We consider four model quasars formed in 10^12-10^13 M_sun halos from different merging histories. Our main results follow. Owing to massive starbursts and funneling of dense gas into the nuclear regions of merging galaxies, the CO is highly excited and the flux density peaks between J=5-8. The CO morphology of z~6 quasars often exhibits multiple emission peaks which arise from H2 concentrations which have not yet fully coalesced. Quasars at z~6 display a large range of sightline dependent line widths such that the lines are narrowest when the rotating H2 gas associated with the quasar is viewed face-on (when L_B is largest), and broadest when the gas is seen edge-on (when L_B is lowest). Thus for all models selection effects exist such that quasars selected for optical luminosity are preferentially face-on which may result in detected CO line widths narrower than the median. The sightline averaged line width is reflective of the circular velocity (V_c) of the host halo, and ranges from sigma~300-650 km/s. For optically selected QSOs, 10-25% (halo-mass dependant) of sightlines have narrow line widths compatible with the sole CO detection at z>6, J1148+5251. When accounting for both the temporal evolution of CO line widths, as well as the redshift evolution of halo V_c, these models self-consistently account for the CO line widths of both z~2 sub-mm galaxies and QSOs. Finally, the dynamical mass derived from the sightline averaged line widths provides a good estimate of the total mass, and allows for a stellar bulge and SMBH consistent with the local M_BH-M_bulge relation. [abridged]