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Sperone Westwater Fischer was founded in 1975, when Italian art dealer Gian Enzo Sperone, Angela Westwater, and German art dealer Konrad Fischer opened a space at 142 Greene Street in SoHo, New York. (The gallery's name was changed to Sperone Westwater in 1982.) An additional space was later established at 121 Greene Street. The founders' original program showcased a European avant-garde alongside a core group of American artists to whom its founders were committed. Notable early exhibitions include a 1977 show of minimalist works by Carl Andre, Dan Flavin, Donald Judd, and Sol Lewitt; seven of Bruce Nauman's seminal early shows; eleven Richard Long exhibitions; and the installation of one of Mario Merz's celebrated glass and neon igloos in 1979 -- part of the gallery's ongoing dedication to Arte Povera artists, including Alighiero Boetti. Other early historical exhibitions at the Greene Street space include a 1989 group show, "Early Conceptual Works," which featured the work of On Kawara, Bruce Nauman, Alighiero Boetti, and Joseph Kosuth, among others; a 1999 Fontana exhibition titled "Gold: Gothic Masters and Lucio Fontana"; and selected presentations of work by Piero Manzoni. From May 2002 to May 2010, the gallery was located at 415 West 13 Street, in a 10,000-square foot space in the Meatpacking District.

In September 2010, Sperone Westwater inaugurated a new Foster + Partners designed building at 257 Bowery in New York. Today, 40 years after its conception, the gallery continues to exhibit an international roster of prominent artists working in a wide variety of media.

In 2011, the Municipal Art Society of New York presented Foster + Partners (with Adamson Associates, architect of record) their MASterworks Award of Best New Building for Sperone Westwater at 257 Bowery. Organized annually by the Municipal Art Society, the MASterworks Awards recognize projects from the preceding year that exemplify excellence in architecture and urban design, and make a significant contribution to New York’s built environment.

In 2012, The Royal Institute of British Architects (RIBA) awarded the building its International Award for architectural excellence.