We measured gill slit fluctuating asymmetry (FA), a measure of developmental noise, in adults of three invertebrate deuterostomes with different feeding modes: the cephalochordate Branchiostoma floridae (an obligate filter feeder), and the enteropneusts Protoglossus graveolens (a facultative filter feeder / deposit feeder) and Saccoglossus bromophenolosus (a deposit feeder). FA was substantially and significantly low in B. floridae and P. graveolens, and high in S. bromophenolosus. Our results suggest that the gills of species that have experienced a relaxation of the filter feeding trait exhibit elevated FA. We found that the timing of development of the secondary collagenous gill bars, compared to the primary gill bars, was highly variable in P. graveolens but not the other two species, demonstrating an independence of gill FA from gill bar heterochrony. We also discovered the occasional ectopic expression of a second set of paired gills posterior to the first set of gills in the enteropneusts, and that these were more common in S. bromophenolosus. Moreover, our finding that gill slits in enteropneusts exhibit bilateral symmetry suggests that the left-sidedness of larval cephalochordate gills, and the directional asymmetry of Cambrian stylophoran echinoderm fossil gills, evolved independently from a bilaterally symmetric ancestor.