Ammonia-oxidizing archaea (AOA) carry out key transformations of ammonia in estuarine systems such as San Francisco Bay (SFB)—the largest estuary on the west coast of North America—and play a significant role in both local and global nitrogen cycling. Using metagenomics and 16S rRNA gene amplicon sequencing, we found that AOA are more abundant than ammonia-oxidizing bacteria and nitrite-oxidizing bacteria, except in the freshwater stations in SFB. Surprisingly, in South SFB we observed recurrent AOA blooms of “Candidatus Nitrosomarinus catalina” SPOT01-like organisms, which account for over 20% of the overall microbial community and co-occur with weeks of high nitrite concentrations (>10 μM) in the oxic water column. We also observed pronounced nitrite peaks occurring in the autumn for 7 of the last 9 years, suggesting that seasonal AOA blooms are common in South SFB. To carefully examine the dynamics and activity of nitrifying microorganisms over the course of an AOA bloom in South SFB, we measured nitrification rates, quantified AOA abundance, and analyzed both metagenomic and metatranscriptomic data during the autumn of 2018 and seasonally throughout 2019. Overall, our study confirms that AOA are not only abundant but also highly active during blooms oxidizing large amounts of ammonia to nitrite—a key intermediate in the microbial nitrogen cycle—and producing reactive compounds that may impact other members of the microbial community.