A 200-foot-long praying mantis that had been trapped in ice for millions of years begins to revive following a volcanic eruption. The military personnel at a military station in northern Canada that monitors information gathered from the Distant Early Warning (DEW) Line realize that the men at one of their outposts are not responding to calls. Commanding officer Col. Joe Parkman flies there to investigate, and finds the post destroyed, its staff gone, and giant slashes in the snow outside.
After an air encounter, Parkman searches the wreckage, and a five-foot-long pointed object in the snow. He takes it to General Mark Ford at the Continental Air Defense Command (ConAD) in Colorado Springs. Ford gathers top scientists, including Professor Anton Gunther, to examine the object, but they fail to identify it. Gunther recommends calling in Dr. Nedrick Jackson, a paleontologist at the Museum of Natural History.
Jackson examines the object and deduces that it is a torn-off spur from an insect's leg, and that it must be from a gigantic praying mantis. In the Arctic, the people of an Eskimo village spot the mantis in the sky, and although they hurry to their boats to escape, it swoops down and kills several men.
Jackson is sent to the northern military installation to investigate further, and discovers that his associate Marge Blaine has obtained permission to accompany him as his photographer. That night, the mantis attacks the building. The full staff of the installation opens fire on the mantis with automatic rifles and a flame-thrower, but it is unscathed and moves away only after planes encircle it.
Later, the base learns that the mantis has attacked a boat off the Canadian coast, which enables Ned to calculate its speed at 200 miles an hour. General Ford calls a press conference to announce the bug's existence, and asks the Ground Observer Corps to track its whereabouts. Ned, Marge and Col. Parkman tirelessly track the bug's progress with the help of military and civilian observers. After wrecking a train, the mantis is sighted in Washington, D.C., atop the Washington Monument.
Parkman and some other pilots attempt to drive the bug toward the sea, but a dense fog throws him off course, and he flies directly into the mantis. As the wounded mantis drops to the ground and crawls into the Manhattan Tunnel, Parkman parachutes to the ground. Ford leads a team that seals off the tunnel, filling it with smoke to provide cover for Joe and his special unit who enter the tunnel armed with rifles and three chemical bombs. Their assault is successful and the mantis is killed.
Later, General Ford, Colonel Parkman, Ned, and Marge enter the tunnel to examine the mantis. Marge photographs its face while the men walk around its side, but Parkman suddenly sees the mantis' arm move, and runs to protect Marge. Ned explains that the movement was merely an autonomic reflex, but Parkman takes the opportunity to pull Marge into an embrace.
- Craig Stevens as Col. Joe Parkman
- William Hopper as Dr. Nedrick Jackson
- Alix Talton as Marge Blaine
- Florenz Ames as Professor Anton Gunther
- Donald Randolph as Major General Mark Ford
- Pat Conway as Sgt. Pete Allen
- Phil Harvey as Lou
- Some of the Arctic scenes in The Deadly Mantis were culled from the 1933 drama SOS Iceberg and a handful of Air Force training films.
- Craig Stevens would later star as Peter Gunn on the popular TV series of the same name.
- Alix Talton was reunited with William Hopper the following year on the Perry Mason TV series episode "The Case of the Long-Legged Models" in the role of Eva Elliot.
- During the movie, the Air Force sends out a message to members of the Ground Observer Corps asking for help in spotting the mantis. This was a real group that existed in two incarnations. The first was during World War Two, and was comprised of civilians who received basic training in spotting and identifying aircraft. It ended in 1944. The GOC was revived in 1950 as part of the Cold War, and was discontinued in 1958 (primarily due to advances in RADAR).
- The Continental Air Defense Command (ConAD) was also referred to in the film The Lost Missile, which became a presentation of The Mads Are Back in 2021.