Cammell Laird laid down Wolverine at Birkenhead in April 1904 as one of three Beagle-class destroyers ordered under the 1908-1909 programme. The Royal Navy gave its builders a loose specification and let each yard interpret it. Laird produced a 266-foot ship with a 28-foot beam, five Yarrow boilers feeding Parsons turbines on three shafts, and 12,500 shaft horsepower. On sea trials in 1910, she hit 27.1 knots and met her contract. She carried one BL 4-inch gun, three 12-pounders, and two 21-inch torpedo tubes - modest armament for a ship whose real weapon was her speed. By November 1913 she had joined the Fifth Destroyer Flotilla in the Mediterranean. When the war came, she was already on station.

August 1914 found Wolverine in the squadron that nearly caught the German battlecruiser Goeben. Rear Admiral Ernest Troubridge deployed eight destroyers, including Wolverine, to help his armoured cruisers cut off Goeben and Breslau before they could escape to Austrian waters. The destroyers had not coaled for a high-speed pursuit. When the Germans turned away, Troubridge left them behind and pressed south with his cruisers - then broke off the chase before dawn, judging Goeben's guns too heavy to engage in daylight. The German ships reached Constantinople and changed the course of the war. Wolverine, denied her quarry, turned to escort and minesweeping work. On 1 November 1914 she helped sink a Turkish armed yacht in the Gulf of Smyrna - her only confirmed kill.

The Dardanelles in spring 1915 was the worst job in the Royal Navy. Wolverine and her sisters towed sweep wires between them, dragging the narrows for mines while Turkish guns on the cliffs above tried to kill them. On 28 April, sweeping in pair with another destroyer, Wolverine took a shell on her bridge. Commander Osmond J. Prentis, her captain, died instantly with two of his men. Two weeks later, on the night of 12-13 May, the pre-dreadnought Goliath was anchored in Morto Bay supporting French troops ashore. Wolverine patrolled the southern straits while Beagle and Bulldog watched the north. The Turkish destroyer Muavenet-i Milliye slipped through the northern picket, torpedoed Goliath, and escaped before Wolverine could close. She would spend the rest of 1915 supporting the Cape Helles landings and the British evacuation that January.

From March 1916, Wolverine ranged the Aegean - the Dodecanese, the Sporades, the Cyclades, the Turkish coast - carrying an unusual passenger. The classical scholar John Myres, an Oxford archaeologist turned naval intelligence officer, had organised irregular bands of Greek and Cretan fighters into a cattle-raiding force. Wolverine ferried them onto Turkish beaches, waited while they stole livestock from Ottoman herds, then carried them back across moonlit water. It was a strange war - half archaeology, half piracy - and it suited the ship well. She was small, fast, and could melt into the Aegean's thousand islands before any pursuit could find her.

In October 1917, the Admiralty recalled Wolverine to home waters. She joined the 2nd Destroyer Flotilla at Buncrana on Lough Swilly, escorting Atlantic convoys through the western approaches where German U-boats hunted hardest. On the night of 12 December, she steamed northwest of Ireland with an escort group bound to meet a Britain-bound convoy. The senior officer aboard the sloop Rosemary ordered a course change. Rosemary's officer of the watch began the manoeuvre too early, then reversed it - putting his ship across Wolverine's bow with no room for either vessel to evade. The sloop struck the destroyer amidships. Wolverine rolled over and went under. The Court of Inquiry blamed Rosemary's bridge crew. Two Wolverine sailors died in the cold Atlantic, three years after the war their ship had outrun across two seas.