BACKGROUND: Termites and their microbial gut symbionts are major recyclers of lignocellulosic biomass. This important symbiosis is obligate but relatively open and more complex in comparison to other well-known insect symbioses such as the strict vertical transmission of Buchnera in aphids. The relative roles of vertical inheritance and environmental factors such as diet in shaping the termite gut microbiome are not well understood. RESULTS: The gut microbiomes of 66 specimens representing seven higher and nine lower termite genera collected in Australia and North America were profiled by small subunit (SSU) rRNA amplicon pyrosequencing. These represent the first reported culture-independent gut microbiome data for three higher termite genera: Tenuirostritermes, Drepanotermes, and Gnathamitermes; and two lower termite genera: Marginitermes and Porotermes. Consistent with previous studies, bacteria comprise the largest fraction of termite gut symbionts, of which 11 phylotypes (6 Treponema, 1 Desulfarculus-like, 1 Desulfovibrio, 1 Anaerovorax-like, 1 Sporobacter-like, and 1 Pirellula-like) were widespread occurring in >/=50% of collected specimens. Archaea are generally considered to comprise only a minority of the termite gut microbiota (<3%); however, archaeal relative abundance was substantially higher and variable in a number of specimens including Macrognathotermes, Coptotermes, Schedorhinotermes, Porotermes, and Mastotermes (representing up to 54% of amplicon reads). A ciliate related to Clevelandella was detected in low abundance in Gnathamitermes indicating that protists were either reacquired after protists loss in higher termites or persisted in low numbers across this transition. Phylogenetic analyses of the bacterial communities indicate that vertical inheritance is the primary force shaping termite gut microbiota. The effect of diet is secondary and appears to influence the relative abundance, but not membership, of the gut communities. CONCLUSIONS: Vertical inheritance is the primary force shaping the termite gut microbiome indicating that species are successfully and faithfully passed from one generation to the next via trophallaxis or coprophagy. Changes in relative abundance can occur on shorter time scales and appear to be an adaptive mechanism for dietary fluctuations.