Outbreaks of respiratory virus infection at mass gatherings pose significant health risks to attendants, host communities and ultimately the global population if they help facilitate viral emergence. However, little is known about the genetic diversity, evolution and patterns of viral transmission during mass gatherings, particularly how much diversity is generated by in situ transmission compared to that imported from other locations. Here we describe the genomic-scale evolution of influenza A viruses sampled from the Hajj at Makkah during 2013-2015. Phylogenetic analysis revealed that the diversity of influenza virus at the Hajj was shaped by multiple introduction events, comprising multiple co-circulating lineages in each year, including those that have circulated in the Middle East and those whose origins likely lie on different continents. At the scale of individual hosts, the majority of minor variants resulted from de novo mutation with only limited evidence of minor variant transmission or minor variants circulating at sub-consensus level despite the likely identification of multiple transmission clusters. Together, these data highlight the complexity of influenza infection at the Hajj, reflecting a mix of global genetic diversity drawn from multiple sources combined with local transmission, and reemphasize the need for vigilant surveillance at mass gatherings.IMPORTANCE Large population sizes and densities at mass gatherings such as the Hajj (Makkah, Saudi Arabia) can contribute to outbreaks of respiratory virus infection by providing local hot-spots for transmission followed by spread to other localities. Using a genome-scale analysis we show that the genetic diversity of influenza A viruses at the Hajj during 2013-2015 was largely shaped by the introduction of multiple viruses from diverse geographic regions, including the Middle East, with only little evidence of inter-host virus transmission at the Hajj and seemingly limited spread of sub-consensus mutational variants. The diversity of viruses at the Hajj highlights the potential for lineage co-circulation during mass gatherings, in turn fuelling segment reassortment and the emergence of novel variants, such that the continued surveillance of respiratory pathogens at mass gatherings should be a public health priority.