It runs entirely within Anne Arundel County, Maryland, for 17.62 miles (28.36 km) from U.S. Route 50/U.S.

I‑97 connects Annapolis with Baltimore/Washington International Airport and links the northern Anne Arundel County communities of Crownsville, Millersville, Severna Park, Glen Burnie, and Ferndale.

It is currently the second shortest primary Interstate Highway in the country after the unfinished I-87 in North Carolina.

I-97 begins at US 50/US 301 (John Hanson Highway), which run concurrently with unsigned I-595, on the edge of the community of Parole west of Annapolis.

The Interstate curves northeast and has a complementary partial interchange with the northern end of MD 3 (Robert Crain Highway).

[2][4] I-97 continues north as a six-lane freeway and is closely paralleled on the east by Veterans Highway on the western edge of Severna Park.

The highways cross the Severn River within Severn Run Natural Environment Area before they diverge slightly at the Interstate's partial cloverleaf interchange with Benfield Boulevard; access from northbound I-97 to the crossroad is via Veterans Highway.

The freeway continues north along the west side of Glen Burnie and meets MD 174 (Quarterfield Road) at a four-ramp partial cloverleaf interchange and MD 100 at a combination interchange that has flyover exit ramps from both directions of I-97.

I-97 continues through Ferndale, where it crosses over the Glen Burnie branch of the Maryland Transit Administration (MTA)'s Baltimore Light RailLink immediately before the highway's four-ramp partial cloverleaf interchange with MD 648 (Baltimore–Annapolis Boulevard), which provides access to the transit line's terminal station, Glen Burnie station.

The Interstate drops to four lanes and reaches its northern terminus just north of the loop ramp from westbound I-695 to I-97 in Brooklyn Park.

The continuation from I-97 includes a ramp to westbound I-695 that allows access to the beltway's interchange with MD 648.

[2] However, the Interstate is dedicated to John A. Cade, who served the area around Severna Park in the Maryland Senate from 1974 to his 1996 death and who worked to secure funding for the highway.

[12] Robert Crain Highway became part of MD 3 in 1927 and then US 301 in 1939 when the US Route was extended from Virginia to Baltimore.

[9] The reconstruction eliminated several dangerous curves, particularly near the Severn River, and expanded the highway from a width of 15 to 20 feet (4.6 to 6.1 m).

[16] The dual roadways and interchange ramps from the southern end of the bypass to MD 648 were constructed starting in March 1955; the concrete-surfaced highway was completed in February 1957.

[21] US 301 was expanded to a divided highway from the southern end of the Glen Burnie Bypass to Benfield in 1956 and 1957.

The highway's second set of lanes, including a new bridge across the Severn River, was constructed and the existing roadway was reconstructed from Benfield to Millersville between 1957 and 1960.

[25] Despite the existence or upcoming construction of two divided highway corridors between Baltimore and Annapolis, a freeway connecting I-695 and US 50 was proposed as early as 1956 in the form of the Arundel Expressway, which would relieve congestion on MD 2.

[30] The 1982 concept of I-68 became unsigned I-595 and I-68 was applied to the National Freeway in Western Maryland in 1991 after AASHTO approved the new designations at its June 1989 meeting.

[37][5] The first section of the highway, from US 50/US 301 to Millersville Road west of the MD 178 interchange, opened in December 1987.

[42] I-97 from its interchange with MD 648 to the new beltway ramps was reconstructed to Interstate Highway standards and expanded to six lanes between May 1993 and August 1995.

[37] The work included the construction of the flyover ramp from northbound I-97 to Veterans Highway just south of MD 3 Bus.

[38][42] The section from north of Benfield Boulevard to MD 178 at Dorrs Corner was reconstructed starting in 1989.

[38][42] In February 1991, the new northbound lanes opened and access from I-97 to Veterans Highway was removed at Dorrs Corner.

[46] The old northbound lanes were reconstructed and repurposed as a two-lane road, Veterans Highway, later that year.

[42][46] Anne Arundel County agreed to accept Veterans Highway for maintenance after the I-97–related construction concluded in a road transfer agreement on July 21, 1988.