In 1860 Walter included Ingleside on a list of his fifty most important works. Apart from its architectural quality (marred by later alterations and additions), Ingleside is significant in Walter's oeuvre because it marks a change in his architecture. Famous as one of the country's leading practitioners of the Greek Revival style, Walter shifted to the modern Italianate style at Ingleside. This change coincided with his Renaissance Revival wing additions to the United States Capitol.

The house's wide and sweeping profile was unusual among American Italianate villas, which tended to be more compact, with the conjunction of two intersecting cubes marked by a square tower. Walter's low rectangular massing was probably a response to the site and to its source. Until its extensive grounds were subdivided in the early 1890s for suburban development, Ingleside sat on the crest of a hill overlooking a varied and rolling landscape that was reputed in the nineteenth century to have been designed by Andrew Jackson Downing. Ingleside's massing and articulation closely resemble those of design 33, “Southern Villa—Romanesque Style,” published in Downing's The Architecture of Country Houses. This relationship can no longer be appreciated fully because the orientation of the house was reversed in the 1896 remodeling by local architect William J. Marsh. The present entrance on the street was originally the garden facade; the terraces and arcaded porticoes date from 1911, changes made by Washington architect Nicholas T. Haller. In their additions, both architects respected Walter's building by conforming to the simple lines of the arched windows and bracketed overhanging eaves of the stuccoed-brick country villa.