When the Royal Navy abandoned Pembroke Dock in 1926, the RAF saw an opportunity. The same deep water that had launched warships could launch flying boats. On 1 January 1930 the air force occupied the former dockyard, and in June 1931 No. 210 Squadron arrived with Supermarine Southamptons - graceful biplane patrol boats with twin engines and open cockpits. Maintenance happened on HMS Flat Iron, a specially-built floating dock that could submerge to let aircraft float onto it, then rise back to hold them out of the water. In 1935 the RAF built its first proper spillway - a sloping ramp that allowed flying boats to be hauled out of the water at any tide. By 1938 the floating dock was redundant and was towed away to Invergordon. The base eventually had two spillways, the longer one 1,121 feet of concrete fitted with a mechanical winch capable of dragging a 25-ton aircraft up out of the haven. A third spillway across the water at Neyland gave the squadrons an alternate landing site when the wind made the south shore unworkable.

In the mid-1930s the Officer Commanding RAF Pembroke Dock was a Wing Commander named Arthur Travers Harris. The world would come to know him as Bomber Harris - the architect of RAF Bomber Command's area bombing campaign against Germany, one of the most controversial commanders of the Second World War. Before all that, he was a man flying patrol boats out of a Welsh estuary. Photographs from the period show him in flying kit on the dockside, ordinary and unsmiling. The decisions he would later make over Hamburg, Cologne, and Dresden lay in front of him. The Sunderland boats he would never get to command grew here too: from 1938 onwards, Short Sunderlands began arriving to replace the older Singapores and Stranraers on Nos. 210 and 228 Squadrons. They would become inseparable from the base.

On 1 June 1940, as the Netherlands fell, several flying boats of the Royal Netherlands Naval Air Service flew west across the North Sea and put down at Pembroke Dock. They became No. 320 (Netherlands) Squadron RAF, eventually moving to nearby RAF Carew Cheriton. Australian, Canadian, and American crews arrived too - the US Navy's VP-63, flying Consolidated PBY Catalinas, was the first US Navy unit to operate in Europe when it reached Pembroke Dock in 1943. The work was unrelenting. Anti-submarine patrols. Convoy escort. Air-sea rescue, equipped with Lindholme Gear - watertight containers of food, water, and a survival raft that could be parachuted to downed crews in the sea. On 2 June 1943 a Sunderland of No. 461 Squadron RAAF - eleven crew, nine Australians and two Britons - was attacked over the Bay of Biscay by eight Junkers Ju 88 fighters while searching for a downed BOAC airliner (whose passenger manifest had included the actor Leslie Howard, killed the day before). The crew shot down three of the Ju 88s. The Sunderland made it home with an airframe described as 'like a colander' from cannon fire, crash-landed at Praa Sands in Cornwall, and was destroyed by the next high tide. There was one fatality among the crew. The rest survived. The action became part of the Sundies' legend.

In 1944 No. 201 Squadron transferred down from RAF Castle Archdale in Northern Ireland to help blockade the western approaches ahead of D-Day, denying U-boats access to the invasion area. The work continued long after the war ended. Three Sunderlands from No. 230 Squadron flew in the 640-aircraft fly-past at the Queen's Coronation Review at RAF Odiham in June 1953, an exact-27-minute aerial spectacle. Through the 1950s, Sunderlands from Nos. 201 and 230 ferried scientists and supplies to the British North Greenland expeditions. When the 1954 expedition returned, No. 230 Squadron brought back the men, the dogs, and adopted a Husky puppy as a mascot. On 28 February 1957 the last flying boat squadrons at Pembroke Dock disbanded. A month later the base went into care-and-maintenance status. Final closure came in 1959, just under thirty years after the RAF first arrived.

In 1963 the French Navy gave a former No. 201 Squadron Sunderland to the town. She sat on the dockside, weathering, until 1971, when she was moved to the RAF Museum at Hendon. The town never quite stopped looking for the others. In 2006 a local fisherman found his lobster pot caught on something deep below the surface. It turned out to be Sunderland T9044, which had sunk in a storm in 1940 and lain in 60 feet of water for sixty-six years. Parts of the airframe have since been recovered and conserved for display. The eastern hangar of RAF Pembroke Dock had one more strange piece of history left in it: in 1979, Marcon Fabrications used it to build the full-scale Millennium Falcon prop for The Empire Strikes Back, a secret project nicknamed the Magic Roundabout. The Pembroke Dock Heritage Centre now occupies the old dockyard chapel and contains a replica Sunderland cockpit with working controls, allowing visitors to fly a simulated patrol over Milford Haven - the route the Mighty Sundies flew, mile after grey mile, watching the west from the air.