I report the first example of communal parasitism in galling aphids and quantify the effects of gall invasion by the inquiline aphid Tamalia inquilina Miller on its host, Tamalia coweni (Cockerell). On populations of the host plants Arctostaphylos spp., both T. coweni and T. inquilina exhibited facultatively communal behavior and co-occupied galls with no apparent agonistic interactions. Although total reproductive output of adult offspring was similar between galls containing T. coweni alone and galls with both species, the allocation of brood was skewed toward that of the inquiline; hence, T. inquilina is a parasite of T. coweni. The presence of T. inquilina had no significant effect on survivorship of T. coweni in mixed-species galls. T. inquilina successfully reproduced in open galls abandoned by T. coweni, and under these circumstances was best characterized as commensal rather than parasitic. My data indicated T. inquilina was significantly more likely to move between galls, supporting the hypothesis that the inquiline actively seeks galls to invade. As frequent occupants of unsealed galls, T. inquilina may incur higher risks of predation and desiccation than T. coweni: experimental evidence showed that at least one specialist predator preferred T. coweni to T. inquilina and that T. inquilina withstood experimental dessication for significantly longer periods than did T. coweni. I suggest the distinctive morphology of T. inquilina is a correlate of the ecology of its parasitic life history on T. coweni.