An accurate force field is essential to computational protein design and protein fold prediction studies. Proper force field tuning is problematic, however, due in part to the incomplete modeling of the unfolded state. Here, we evaluate and optimize a protein design force field by constraining the amino acid composition of the designed sequences to that of a well behaved model protein. According to the random energy model, unfolded state energies are dependent only on amino acid composition and not the specific arrangement of amino acids. Therefore, energy discrepancies between computational predictions and experimental results, for sequences of identical composition, can be directly attributed to flaws in the force field's ability to properly account for folded state sequence energies. This aspect of fixed composition design allows for force field optimization by focusing solely on the interactions in the folded state. Several rounds of fixed composition optimization of the 56-residue beta1 domain of protein G yielded force field parameters with significantly greater predictive power: Optimized sequences exhibited higher wild-type sequence identity in critical regions of the structure, and the wild-type sequence showed an improved Z-score. Experimental studies revealed a designed 24-fold mutant to be stably folded with a melting temperature similar to that of the wild-type protein. Sequence designs using engrailed homeodomain as a scaffold produced similar results, suggesting the tuned force field parameters were not specific to protein G.