This cozy 448 square foot home at 2724 Q Street (built 1920) has to be in the running for smallest house in Richmond. The property last sold in 1994 for $3,500.

A 315 square foot house on Nine Mile was demolished in 2014. A 576 square foot house on 1st Avenue sold for $38,000 in 2016.

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UPDATE from the comments:

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1902 Lynhaven Ave. (357 sq ft) via @jtknopf: