It was incorporated in 1846 as a branch off the Old Colony Railroad main line from Boston to Plymouth.

In 1854 an extension of approximately 0.5 miles (0.80 km) west-southwest was proposed, which would have extended the line from the Mattapan to a connection with the Boston and New York Central railroad (today's Fairmount Line) approximately midway between today's Blue Hill Avenue station and the River Street crossing.

From 1848 to 1872, commuter rail service to Ashmont operated over the whole line (as the Milton Branch).

From Shawmut Junction to Central Avenue, the trail shares the corridor with the MBTA trolley line, and occupies only the former northern freight track.

Media related to Dorchester and Milton Branch Railroad at Wikimedia Commons