The mechanisms of aging that are involved in the development of idiopathic pulmonary fibrosis (IPF) are still unclear. Although it has been hypothesized that the proliferation and activation of human lung fibroblasts (hLF) are essential in IPF, no studies have assessed how this process works in an aging lung. Our goal was to elucidate if there were age-related changes on primary hLF isolated from IPF lungs compared to age-matched controls. We investigated several hallmarks of aging in hLF from IPF patients and age-matched controls. IPF hLF have increased cellular senescence with higher expression of β-galactosidase, p21, p16, p53 and cytokines related to the senescence-associated secretory phenotype (SASP) as well as decreased proliferation/apoptosis compared to age-match controls. Additionally, we observed shorter telomeres, mitochondrial dysfunction, and upon TGF-β stimulation, increased markers of ER stress. Our data suggests that IPF hLF develop senescence resulting in a decreased apoptosis and that the development of SASP may be an important contributor to the fibrotic process observed in IPF. These results might change the existing paradigm, which describes fibroblasts as aberrantly activated cells, to a cell with a senescence phenotype.