Route 40 also serves as the primary access to St. John's International Airport and the Bell Island Ferry terminal.

Route 40 begins as a two-lane street just north of downtown St. John's at an intersection with Rennies Mill Road.

Route 40 now widens to a 4-lane highway as it passes through a business district and has an intersection with The Parkway (Prince Philip Drive/MacDonald Drive).

It continues northwest to have a large interchange with Route 1 (Trans Canada Highway, exits 47 A/B) before passing by St. John's International Airport.

The highway now narrows to 2-lanes to leave St. John's and pass through rural areas to enter Portugal Cove-St. Phillips.