Secondary immune events likely aggravate Covid-19 pathology. In inflammation and homeostasis macrophages are indispensable regulators of pulmonary tissue integrity. We investigated pulmonary macrophage states in two independent cohorts of patients suffering from Covid-19 ARDS employing functional single cell transcriptomics and multiplexed histopathological methods. CD163+ macrophage numbers were increased in lung tissues of deceased Covid-19 patients. Transcriptomes of broncheoalveolar lavage macrophages dispersed in between 3 poles in integrated gene spaces. Next to a monocytic pole, Macrophages were either mainly of conventional alveolar macrophage differentiation with elevated lipid/cholesterol processing, or exhibited a third gene profile, of likely recent hematopoietic origin. Strikingly, these CD163+/LGMN+ cells highly expressed gene signatures of macrophage polarizations found in pulmonary fibrotic disease such as Idiopathic Pulmonary Fibrosis (IPF). Furthermore, in primary human in-vitro cultured monocytes, SARS-CoV-2 co-incubation directly induced the expression of these fibrosis-associated programs, which were distinct from inflammatory or antiviral responses. These findings were present in proteomic as well as single cell transcriptomic analyses. Moreover, we present radiological, ultra-structural, and lung mechanical evidence of Covid-19-triggered pulmonary fibrosis. In conclusion, macrophages in pulmonary tissue of Covid-19 ARDS patients expressed fibrosis-associated gene modules which were inducible by direct in-vitro stimulation of monocytes with SARS-CoV-2.