Mechanical frequency combs are poised to bring the applications and utility of optical frequency combs into the mechanical domain. So far, their main challenge has been strict requirements on drive frequencies and power, which complicate operation. We demonstrate a straightforward mechanism to create a frequency comb consisting of mechanical overtones (integer multiples) of a single eigenfrequency, by monolithically integrating a suspended dielectric membrane with a counter-propagating optical trap. The periodic optical field modulates the dielectrophoretic force on the membrane at the overtones of a membrane’s motion. These overtones share a fixed frequency and phase relation, and constitute a mechanical frequency comb. The periodic optical field also creates an optothermal parametric drive that requires no additional power or external frequency reference. This combination of effects results in an easy-to-use mechanical frequency comb platform that requires no precise alignment, no additional feedback or control electronics, and only uses a single, mW continuous wave laser beam. This highlights the overtone frequency comb as the straightforward future for applications in sensing, metrology and quantum acoustics.