Microscopic many-body theory coupled with Maxwell's equation is used to study dual-wavelength operation in vertical external-cavity surface-emitting lasers. The intrinsically dynamic nature of coexisting emission wavelengths in semiconductor lasers is associated with characteristic non-equilibrium carrier dynamics, which causes significant deformations of the quasi-equilibrium gain and carrier inversion. Extended numerical simulations are employed to efficiently investigate the parameter space to identify the regime for dual-wavelength operation. Using a frequency selective intracavity etalon, two families of modes are stabilized with dynamical interchange of the strongest emission peaks. For this operation mode, anti-correlated intensity noise is observed in agreement with the experiment. A method using effective frequency selective filtering is suggested for stabilization of genuine dual-wavelength output.