We used a combination of metatranscriptomic analyses and quantitative PCR (qPCR) to study seasonal changes in Thaumarchaeota populations from a salt marsh-dominated estuary. Surface waters (0.5 m depth) were sampled quarterly at Marsh Landing, Sapelo Island, GA, USA over a 3-year period. We found a mid-summer peak in Thaumarchaeota abundance measured by qPCR of either 16S rRNA or amoA genes in each of the 3 years. Thaumarchaeota were 100–1000-fold more abundant during the peak than at other times of the year, whereas the abundance of ammonia- and nitrite-oxidizing Bacteria varied <10-fold over the same period. Analysis of the microdiversity of several highly transcribed genes in 20 metatranscriptomes from a 1-year subset of these samples showed that the transcriptionally active population consisted of 2 or 3 dominant phylotypes that differed between successive summers. This shift appeared to have begun during the preceding winter and spring. Transcripts from the same genes dominated the Thaumarchaeota mRNA pool throughout the year, with genes encoding proteins believed to be involved in nitrogen uptake and oxidation, and two hypothetical proteins being the most abundant transcripts in all libraries. Analysis of individual genes over the seasonal cycle suggested that transcription was tied more closely to variation in growth rates than to seasonal changes in environmental conditions. Day–night differences in the relative abundance of transcripts for ribosomal proteins suggested diurnal variation in Thaumarchaeota growth.