His apprenticeship there coincided with several important Chicago School architects including Frank Lloyd Wright.

The two formed a firm named "Falkenham & Gill, the Architects", and completed several projects, including some large commercial buildings.

In the late 1890s, Gill's designs began to use concrete more heavily, and his work in that medium contributed significantly to its use in the future.

In this period, Gill trained Hazel Wood Waterman, who helped with a group of houses built near Balboa Park for socialites Alice Lee and Katherine Teats.

Gill's design was chosen in a competition among professional architects, and was one of the first projects in the country to combine water and colored electrical light effects.

Gill returned to live in North San Diego County in the 1920s, but his pace of work slowed considerably due to lingering illness, changing public tastes, and his diminishing willingness to compromise with clients.

His last contract was to create houses for several displaced Native American families who would then settle at the Rancho Barona Indian Reservation near Lakeside, California.

[2] Irving Gill was concerned with the social impact of good architecture and approached his projects with equal skill and interest, whether he was designing for bankers and mayors or for Indian reservations, an African American church, or migrant Mexican workers and their children.

His houses are known for minimal or flush mouldings; simple (or no) fireplace mantles; coved, and therefore fluid, floor-to-wall transitions; enclosed-side bathtubs; plentiful skylights;, plastered walls with only occasional, but featured, wood elements; flush five-piece doors; concrete or Sorel cement floors; and a general avoidance of dividing lines, ledges, and unnecessary material changes.

According to Joseph Giovannini, "the desire for an easily maintained, sanitary home drove Gill's aesthetic toward purity.

"[7] Gill's aesthetically best work, much of it dating from the 1910s, favors flat roofs without eaves, a unity of materials (mostly concrete), casement windows with transoms, white or near-white exterior and interior walls, cubic or rectangular massing, plentiful ground-level arches or series of arches creating transitional breezeways in the manner of the California missions.

His best-known work still in active use today includes the Ellen Browning Scripps residence (now the Museum of Contemporary Art San Diego), the earliest buildings of The Bishop's School, the La Jolla Woman's Club, the La Jolla Recreation Center and the George W. Marston House.

Gill's reputation did quickly fade after his death, and it languished until he was included in the 1960 book Five California Architects by Esther McCoy and Randell L. Makinson.

While some have speculated that the marriage was unsuccessful, a few remaining letters in Gill's own hand indicate his deep and fond feelings for his wife.