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The first series of robots were originally designed and built by Spencer Smythe with the financial backing of J. Jonah Jameson who piloted them for the pleasure of personally hunting the superhero he hated for capture. However, Spider-Man always managed to defeat each robot in turn. Smythe's continual efforts to perfect his machines backfired on him, leading to himself being fatally contaminated by radiation poisoning from the building materials of his creations. Blaming both Jameson and Spider-Man for this, he attempted, as a final act, to murder them both, but died just before Spider-Man thwarted the attempt.
Later, Jameson commissioned another scientist, Dr. Marla Madison, to create a new and improved Spider-Slayer. While that attempt failed, he eventually fell in love with her and married her (Amazing Spider-Man #167-168).In Amazing Spider-Man Annual #19 (1985), Smythe's son, Alistair, emerged as the new builder of Spider-Slayers. He swore revenge on Spider-Man, repeatedly attacking the superhero with his own series of Slayers. Smythe later mutated into a humanoid Spider-Slayer, but remains a minor foe.
The original Spider-Slayer was seen among the robots and machines in Tinkerer's collection. Wolverine later destroyed the Spider-Slayer when Tinkerer attempted to use it against him. It was later used by J. Jonah Jameson to attack She-Hulk after she had married his son John, but it was destroyed.