After Brinson, the route curves northeast, and then northwest, to meet its northern terminus, an intersection with US 27/SR 1 in Colquitt.

In 1965, a new route was constructed in Miller County, extending from the SR 310 stub end north to Colquitt.

When the Miller County section was commissioned, SR 310 was at maximum length, extending nearly 33 miles (53 km).

That year, the 5.8-mile (9.3 km) dead end Yates Spring Road section south of SR 253 to Lake Seminole was decommissioned and the 3.5-mile (5.6 km) portion of the highway on the other side of the lake was changed to SR 97 Spur.

The northern terminus of the highway was relocated within Colquitt to Grow Street instead of connecting to US 27 in downtown.