The highway's southern terminus lies at the shores of the Pasquotank River near its mouth with the Albemarle Sound.

NC 344 winds northwestward through rural Pasquotank County and the unincorporated community of Weeksville as the two-lane Salem Church and Weeksville Roads, becoming a four-lane with center turning lane thoroughfare at the main gate of Coast Guard Air Station Elizabeth City southeast of Elizabeth City.

Continuing past mainline US 17 as the limited-access thoroughfare Halstead Boulevard Extension, NC 344 travels through the heart of an emerging retail corridor in western Elizabeth City before coming to a diamond interchange at US 17 Bypass.

The previously unsigned Halstead Boulevard had become a major commercial corridor along the south side of Elizabeth City starting in the early 1990s.

North Carolina Highway 170 (NC 170) was established in 1935 as a new primary routing, from US 17, in Elizabeth City, south to Weeksville.