Many viruses form highly pleomorphic particles. In influenza, virion structure is of interest not only in the context of virus assembly, but also because pleomorphic variations may correlate with infectivity and pathogenicity. We have used fluorescence super-resolution microscopy combined with a rapid automated analysis pipeline, a method well-suited to the study of large numbers of pleomorphic structures, to image many thousands of individual influenza virions; gaining information on their size, morphology and the distribution of membrane-embedded and internal proteins. We observed broad phenotypic variability in filament size, and Fourier transform analysis of super resolution images demonstrated no generalized common spatial frequency patterning of HA or NA on the virion surface, suggesting a model of virus particle assembly where the release of progeny filaments from cells occurs in a stochastic way. We also showed that viral RNP complexes are located preferentially within Archetti bodies when these were observed at filament ends, suggesting that these structures may play a role in virus transmission. Our approach therefore offers exciting new insights into influenza virus morphology and represents a powerful technique that is easily extendable to the study of pleomorphism in other pathogenic viruses. Author summary: Viruses are significant human pathogens. In influenza, virus structure and morphology has been linked to pathogenicity; however commonly used methods to study virus structure are often low through-put, or lack the resolution required to resolve virus particle features. In addition, influenza filaments are frequently understudied due to their fragile nature and loss of filamentous morphology during viral passage. In order to address this, we have developed a fluorescence super-resolution microscopy and rapid automated analysis pipeline to image many thousands of individual influenza virions at a time, gaining information on their size, morphology and protein distribution. Using this method we were able to show that there is no specific alternation of the surface glycoproteins in filaments, and that neuraminidase-enriched Archetti bodies preferentially house viral ribonucleoprotein complexes. Our findings offer new insights into influenza virus particle assembly and virus transmission, and further, our versatile methods have the potential to contribute towards multiple areas of virus research. [ABSTRACT FROM AUTHOR]