Early and mid-career (1925–1950)
Between 1925 and 1926, Albright's mature "baroque" formal style began to emerge, and in many cases the general public was not prepared for his "naked and uncompromising disclosure of the human condition." At the end of 1926, Albright and his brother spent three months in southern California near San Diego. While there, Albright produced several works that are representative of the maturity of his style, including I Walk To and Fro Through Civilization and I Talk As I Walk (Follow Me, The Monk) and I Drew a Picture in the Sand and the Water Washed It Away (The Theosophist). By 1927, he and Malvin returned to Illinois where their father Adam had repurposed an old Methodist church for use as the Albright Gallery of Painting and Sculpture. Due to the brothers’ proximity for the next two years, Malvin adopted the pseudonym Zsissly to avoid confusion with Ivan. It was during the years at this studio that Ivan's style began to cause controversy: In May 1928 his painting The Lineman was used as the cover for the trade magazine Electric Light and Power. The magazine's readership thought the figure of the lineman was inaccurate and depressing; however, the painting was far more successful with art critics. Not long after, Albright began working on paintings that emphasized the microscopic quality of surface as much as baroque form, beginning with Woman (1928). When Woman was displayed at the Toledo Museum of Art in the 17th Exhibition of Selected Paintings by Contemporary American Artists in 1929, the painting was met with protesters who first had the painting removed, followed by another group protesting the painting's removal.
By 1931 and the onset of the Great Depression, Albright's career was becoming established. In July of that year he exhibited fourteen paintings at the Art Institute of Chicago alongside fellow artists George and Martin Baer. That year as well, following the completion of the monumental Into the World There Came a Soul Called Ida (1929–30), he began his decade-long obsession with his magnum-opus That Which I Should Have Done I Did Not Do (The Door) (1931). According to Albright, the Depression didn't significantly affect his career because people didn't buy his paintings "whether times were good or bad, [so] it didn’t make a bit of difference." Indeed, his father's success in art sales and real estate allowed Albright to live comfortably through the 1930s. Nonetheless, as did many other artists of the period, Albright participated in the Public Works of Art Project in Illinois. He was supposed to receive thirty-eight dollars per week in the program as a "class A" artist, but he maintained that he never received payment for his works. While in the project, Albright completed two paintings: The Farmer's Kitchen (1933–34) and Self-Portrait (1934). The Farmer's Kitchen, now housed at the Smithsonian American Art Museum, in particular suited the PWAP's expectations of images of hard-working Americans and is indeed thematically the closest of Albright's paintings to those of the popular Regionalists. The subject nonetheless allowed Albright to display in the woman weariness and deterioration and thus to critique the positivist outlook of Regionalist artists like Grant Wood and Doris Lee.
The 1940s brought a series of changes in Albright's life. His mother, Carla Wilson Albright, died on May 8, 1939, and heartbroken, he, Malvin and Adam spent the next several summers painting in Maine. During this period, in 1941, Albright completed work on The Door and began work on its de facto companion Poor Room – There Is No Time, No End, No Today, No Yesterday, No Tomorrow, Only the Forever and Forever and Forever Without End (The Window), which Albright would continue to work on off-and-on for the next twenty-one years. Work on The Window experienced its first interruption when Ivan and Malvin were asked to paint for the Metro-Goldwyn-Mayer adaptation of The Picture of Dorian Gray, directed by Albert Lewin. For his portrait, Albright insisted on working under the same harsh lights as on the set, so to compensate he developed a new aggressive sensibility around color that would persist in his work into the 1970s. In 1946, Albright's personal life changed even more when on August 27 he married Josephine Medill Patterson Reeve. After the marriage, the couple briefly moved to Billings, Montana and then south to Ten Sleep, Wyoming before returning to Chicago. Albright adopted Josephine's children upon the marriage. In 1947 Ivan and Josephine had a son Adam Medill, and two years following in 1949, they had a daughter Blandina Van Etten.