The parkway was originally built in 1929 as a connector between NY 27A and the newly opened Heckscher (formerly Deer Range) State Park.

The Long Island Transportation Plan 2000, a long-term study done in the late 1990s, called for the Heckscher Parkway to be widened west of NY 27 to accommodate a carpool and bus lane.

After the interchange, the parkway continues generally eastward through Brentwood, running past dense woods buffering the highway from more developed areas.

Past Sunrise Highway, the Heckscher State Parkway enters East Islip, crossing over Long Island Rail Road's Montauk Branch at a point just west of the Great River station.

[2] On the other side of the tracks, the parkway begins to run along the western edge of Bayard Cutting Arboretum State Park while crossing over CR 50 (Union Boulevard).

The parkway intersects Timber Point Road at exit 46 before ending shortly afterward at the tollbooth for Heckscher State Park.

While the parkway designation ends here, the highway's right-of-way continues southwest into the park, 8.52 miles (13.71 km) from the Southern State.

Their representatives in the New York State Legislature refused to provide money for a park, leading a group to contact August Heckscher, a local philanthropist.

A motorcade of 110 vehicles followed the new parkway to the Bayard Cutting Arboretum, but Governor Rockfeller was late due to mechanical difficulties with his personal plane.

The new parkway led to the expansion of facilities along the road, which included an additional 1,658 acres (671 ha) of land and 18,000 feet (5,500 m) of new beachfront.

Opening the parkway also created connections to the nearby Southside Sportsmen's Club, which would be turned into a recreation area, and the Bayard Cutting Arboretum.