diff --git a/storage_controller/src/id_lock_map.rs b/storage_controller/src/id_lock_map.rs
index fcd3eb57e25f..2d8b674f861b 100644
--- a/storage_controller/src/id_lock_map.rs
+++ b/storage_controller/src/id_lock_map.rs
@@ -112,6 +112,14 @@ where
         }
     }
 
+    pub(crate) fn try_exclusive(&self, key: T, operation: I) -> Option<TracingExclusiveGuard<I>> {
+        let mut locked = self.entities.lock().unwrap();
+        let entry = locked.entry(key).or_default().clone();
+        let mut guard = TracingExclusiveGuard::new(entry.try_write_owned().ok()?);
+        *guard.guard = Some(operation);
+        Some(guard)
+    }
+
     /// Rather than building a lock guard that re-takes the [`Self::entities`] lock, we just do
     /// periodic housekeeping to avoid the map growing indefinitely
     pub(crate) fn housekeeping(&self) {
diff --git a/storage_controller/src/persistence.rs b/storage_controller/src/persistence.rs
index cc377e606ee8..c5eb106f24ef 100644
--- a/storage_controller/src/persistence.rs
+++ b/storage_controller/src/persistence.rs
@@ -97,6 +97,7 @@ pub(crate) enum DatabaseOperation {
     TenantGenerations,
     ShardGenerations,
     ListTenantShards,
+    LoadTenant,
     InsertTenantShards,
     UpdateTenantShard,
     DeleteTenant,
@@ -330,11 +331,40 @@ impl Persistence {
 
     /// At startup, load the high level state for shards, such as their config + policy.  This will
     /// be enriched at runtime with state discovered on pageservers.
-    pub(crate) async fn list_tenant_shards(&self) -> DatabaseResult<Vec<TenantShardPersistence>> {
+    ///
+    /// We exclude shards configured to be detached.  During startup, if we see any attached locations
+    /// for such shards, they will automatically be detached as 'orphans'.
+    pub(crate) async fn load_active_tenant_shards(
+        &self,
+    ) -> DatabaseResult<Vec<TenantShardPersistence>> {
+        use crate::schema::tenant_shards::dsl::*;
         self.with_measured_conn(
             DatabaseOperation::ListTenantShards,
             move |conn| -> DatabaseResult<_> {
-                Ok(crate::schema::tenant_shards::table.load::<TenantShardPersistence>(conn)?)
+                let query = tenant_shards.filter(
+                    placement_policy.ne(serde_json::to_string(&PlacementPolicy::Detached).unwrap()),
+                );
+                let result = query.load::<TenantShardPersistence>(conn)?;
+
+                Ok(result)
+            },
+        )
+        .await
+    }
+
+    /// When restoring a previously detached tenant into memory, load it from the database
+    pub(crate) async fn load_tenant(
+        &self,
+        filter_tenant_id: TenantId,
+    ) -> DatabaseResult<Vec<TenantShardPersistence>> {
+        use crate::schema::tenant_shards::dsl::*;
+        self.with_measured_conn(
+            DatabaseOperation::LoadTenant,
+            move |conn| -> DatabaseResult<_> {
+                let query = tenant_shards.filter(tenant_id.eq(filter_tenant_id.to_string()));
+                let result = query.load::<TenantShardPersistence>(conn)?;
+
+                Ok(result)
             },
         )
         .await
diff --git a/storage_controller/src/service.rs b/storage_controller/src/service.rs
index 359fcb3288e3..fd4ee7fd101e 100644
--- a/storage_controller/src/service.rs
+++ b/storage_controller/src/service.rs
@@ -155,6 +155,7 @@ enum TenantOperations {
     TimelineArchivalConfig,
     TimelineDetachAncestor,
     TimelineGcBlockUnblock,
+    DropDetached,
 }
 
 #[derive(Clone, strum_macros::Display)]
@@ -416,8 +417,8 @@ pub struct Service {
     /// Queue of tenants who are waiting for concurrency limits to permit them to reconcile
     /// Send into this queue to promptly attempt to reconcile this shard next time units are available.
     ///
-    /// Note that this state logically lives inside ServiceInner, but carrying Sender here makes the code simpler
-    /// by avoiding needing a &mut ref to something inside the ServiceInner.  This could be optimized to
+    /// Note that this state logically lives inside ServiceState, but carrying Sender here makes the code simpler
+    /// by avoiding needing a &mut ref to something inside the ServiceState.  This could be optimized to
     /// use a VecDeque instead of a channel to reduce synchronization overhead, at the cost of some code complexity.
     delayed_reconcile_tx: tokio::sync::mpsc::Sender<TenantShardId>,
 
@@ -1165,6 +1166,20 @@ impl Service {
             }
         }
 
+        // If we just finished detaching all shards for a tenant, it might be time to drop it from memory.
+        if tenant.policy == PlacementPolicy::Detached {
+            // We may only drop a tenant from memory while holding the exclusive lock on the tenant ID: this protects us
+            // from concurrent execution wrt a request handler that might expect the tenant to remain in memory for the
+            // duration of the request.
+            let guard = self.tenant_op_locks.try_exclusive(
+                tenant.tenant_shard_id.tenant_id,
+                TenantOperations::DropDetached,
+            );
+            if let Some(guard) = guard {
+                self.maybe_drop_tenant(tenant.tenant_shard_id.tenant_id, &mut locked, &guard);
+            }
+        }
+
         // Maybe some other work can proceed now that this job finished.
         if self.reconciler_concurrency.available_permits() > 0 {
             while let Ok(tenant_shard_id) = locked.delayed_reconcile_rx.try_recv() {
@@ -1294,7 +1309,7 @@ impl Service {
             .set(nodes.len() as i64);
 
         tracing::info!("Loading shards from database...");
-        let mut tenant_shard_persistence = persistence.list_tenant_shards().await?;
+        let mut tenant_shard_persistence = persistence.load_active_tenant_shards().await?;
         tracing::info!(
             "Loaded {} shards from database.",
             tenant_shard_persistence.len()
@@ -1546,8 +1561,14 @@ impl Service {
         // the pageserver API (not via this service), we will auto-create any missing tenant
         // shards with default state.
         let insert = {
-            let locked = self.inner.write().unwrap();
-            !locked.tenants.contains_key(&attach_req.tenant_shard_id)
+            match self
+                .maybe_load_tenant(attach_req.tenant_shard_id.tenant_id, &_tenant_lock)
+                .await
+            {
+                Ok(_) => false,
+                Err(ApiError::NotFound(_)) => true,
+                Err(e) => return Err(e.into()),
+            }
         };
 
         if insert {
@@ -2439,6 +2460,99 @@ impl Service {
         }
     }
 
+    /// For APIs that might act on tenants with [`PlacementPolicy::Detached`], first check if
+    /// the tenant is present in memory. If not, load it from the database.  If it is found
+    /// in neither location, return a NotFound error.
+    ///
+    /// Caller must demonstrate they hold a lock guard, as otherwise two callers might try and load
+    /// it at the same time, or we might race with [`Self::maybe_drop_tenant`]
+    async fn maybe_load_tenant(
+        &self,
+        tenant_id: TenantId,
+        _guard: &TracingExclusiveGuard<TenantOperations>,
+    ) -> Result<(), ApiError> {
+        let present_in_memory = {
+            let locked = self.inner.read().unwrap();
+            locked
+                .tenants
+                .range(TenantShardId::tenant_range(tenant_id))
+                .next()
+                .is_some()
+        };
+
+        if present_in_memory {
+            return Ok(());
+        }
+
+        let tenant_shards = self.persistence.load_tenant(tenant_id).await?;
+        if tenant_shards.is_empty() {
+            return Err(ApiError::NotFound(
+                anyhow::anyhow!("Tenant {} not found", tenant_id).into(),
+            ));
+        }
+
+        // TODO: choose a fresh AZ to use for this tenant when un-detaching: there definitely isn't a running
+        // compute, so no benefit to making AZ sticky across detaches.
+
+        let mut locked = self.inner.write().unwrap();
+        tracing::info!(
+            "Loaded {} shards for tenant {}",
+            tenant_shards.len(),
+            tenant_id
+        );
+
+        locked.tenants.extend(tenant_shards.into_iter().map(|p| {
+            let intent = IntentState::new();
+            let shard =
+                TenantShard::from_persistent(p, intent).expect("Corrupt shard row in database");
+
+            // Sanity check: when loading on-demand, we should always be loaded something Detached
+            debug_assert!(shard.policy == PlacementPolicy::Detached);
+            if shard.policy != PlacementPolicy::Detached {
+                tracing::error!(
+                    "Tenant shard {} loaded on-demand, but has non-Detached policy {:?}",
+                    shard.tenant_shard_id,
+                    shard.policy
+                );
+            }
+
+            (shard.tenant_shard_id, shard)
+        }));
+
+        Ok(())
+    }
+
+    /// If all shards for a tenant are detached, and in a fully quiescent state (no observed locations on pageservers),
+    /// and have no reconciler running, then we can drop the tenant from memory.  It will be reloaded on-demand
+    /// if we are asked to attach it again (see [`Self::maybe_load_tenant`]).
+    ///
+    /// Caller must demonstrate they hold a lock guard, as otherwise it is unsafe to drop a tenant from
+    /// memory while some other function might assume it continues to exist while not holding the lock on Self::inner.
+    fn maybe_drop_tenant(
+        &self,
+        tenant_id: TenantId,
+        locked: &mut std::sync::RwLockWriteGuard<ServiceState>,
+        _guard: &TracingExclusiveGuard<TenantOperations>,
+    ) {
+        let mut tenant_shards = locked.tenants.range(TenantShardId::tenant_range(tenant_id));
+        if tenant_shards.all(|(_id, shard)| {
+            shard.policy == PlacementPolicy::Detached
+                && shard.reconciler.is_none()
+                && shard.observed.is_empty()
+        }) {
+            let keys = locked
+                .tenants
+                .range(TenantShardId::tenant_range(tenant_id))
+                .map(|(id, _)| id)
+                .copied()
+                .collect::<Vec<_>>();
+            for key in keys {
+                tracing::info!("Dropping detached tenant shard {} from memory", key);
+                locked.tenants.remove(&key);
+            }
+        }
+    }
+
     /// This API is used by the cloud control plane to migrate unsharded tenants that it created
     /// directly with pageservers into this service.
     ///
@@ -2465,14 +2579,26 @@ impl Service {
         )
         .await;
 
-        if !tenant_shard_id.is_unsharded() {
+        let tenant_id = if !tenant_shard_id.is_unsharded() {
             return Err(ApiError::BadRequest(anyhow::anyhow!(
                 "This API is for importing single-sharded or unsharded tenants"
             )));
-        }
+        } else {
+            tenant_shard_id.tenant_id
+        };
+
+        // In case we are waking up a Detached tenant
+        match self.maybe_load_tenant(tenant_id, &_tenant_lock).await {
+            Ok(()) | Err(ApiError::NotFound(_)) => {
+                // This is a creation or an update
+            }
+            Err(e) => {
+                return Err(e);
+            }
+        };
 
         // First check if this is a creation or an update
-        let create_or_update = self.tenant_location_config_prepare(tenant_shard_id.tenant_id, req);
+        let create_or_update = self.tenant_location_config_prepare(tenant_id, req);
 
         let mut result = TenantLocationConfigResponse {
             shards: Vec::new(),
@@ -2600,6 +2726,8 @@ impl Service {
         let tenant_id = req.tenant_id;
         let patch = req.config;
 
+        self.maybe_load_tenant(tenant_id, &_tenant_lock).await?;
+
         let base = {
             let locked = self.inner.read().unwrap();
             let shards = locked
@@ -2644,19 +2772,7 @@ impl Service {
         )
         .await;
 
-        let tenant_exists = {
-            let locked = self.inner.read().unwrap();
-            let mut r = locked
-                .tenants
-                .range(TenantShardId::tenant_range(req.tenant_id));
-            r.next().is_some()
-        };
-
-        if !tenant_exists {
-            return Err(ApiError::NotFound(
-                anyhow::anyhow!("Tenant {} not found", req.tenant_id).into(),
-            ));
-        }
+        self.maybe_load_tenant(req.tenant_id, &_tenant_lock).await?;
 
         self.set_tenant_config_and_reconcile(req.tenant_id, req.config)
             .await
@@ -2949,6 +3065,8 @@ impl Service {
         let _tenant_lock =
             trace_exclusive_lock(&self.tenant_op_locks, tenant_id, TenantOperations::Delete).await;
 
+        self.maybe_load_tenant(tenant_id, &_tenant_lock).await?;
+
         // Detach all shards. This also deletes local pageserver shard data.
         let (detach_waiters, node) = {
             let mut detach_waiters = Vec::new();
@@ -3068,6 +3186,8 @@ impl Service {
         )
         .await;
 
+        self.maybe_load_tenant(tenant_id, &_tenant_lock).await?;
+
         failpoint_support::sleep_millis_async!("tenant-update-policy-exclusive-lock");
 
         let TenantPolicyRequest {
@@ -5150,11 +5270,13 @@ impl Service {
             )));
         }
 
-        let mut shards = self.persistence.list_tenant_shards().await?;
-        shards.sort_by_key(|tsp| (tsp.tenant_id.clone(), tsp.shard_number, tsp.shard_count));
+        let mut persistent_shards = self.persistence.load_active_tenant_shards().await?;
+        persistent_shards
+            .sort_by_key(|tsp| (tsp.tenant_id.clone(), tsp.shard_number, tsp.shard_count));
+
         expect_shards.sort_by_key(|tsp| (tsp.tenant_id.clone(), tsp.shard_number, tsp.shard_count));
 
-        if shards != expect_shards {
+        if persistent_shards != expect_shards {
             tracing::error!("Consistency check failed on shards.");
             tracing::error!(
                 "Shards in memory: {}",
@@ -5163,7 +5285,7 @@ impl Service {
             );
             tracing::error!(
                 "Shards in database: {}",
-                serde_json::to_string(&shards)
+                serde_json::to_string(&persistent_shards)
                     .map_err(|e| ApiError::InternalServerError(e.into()))?
             );
             return Err(ApiError::InternalServerError(anyhow::anyhow!(
@@ -6119,6 +6241,10 @@ impl Service {
         let mut pending_reconciles = 0;
         let mut az_violations = 0;
 
+        // If we find any tenants to drop from memory, stash them to offload after
+        // we're done traversing the map of tenants.
+        let mut drop_detached_tenants = Vec::new();
+
         let mut reconciles_spawned = 0;
         for shard in tenants.values_mut() {
             // Accumulate scheduling statistics
@@ -6152,6 +6278,25 @@ impl Service {
                 // Shard wanted to reconcile but for some reason couldn't.
                 pending_reconciles += 1;
             }
+
+            // If this tenant is detached, try dropping it from memory. This is usually done
+            // proactively in [`Self::process_results`], but we do it here to handle the edge
+            // case where a reconcile completes while someone else is holding an op lock for the tenant.
+            if shard.tenant_shard_id.shard_number == ShardNumber(0)
+                && shard.policy == PlacementPolicy::Detached
+            {
+                if let Some(guard) = self.tenant_op_locks.try_exclusive(
+                    shard.tenant_shard_id.tenant_id,
+                    TenantOperations::DropDetached,
+                ) {
+                    drop_detached_tenants.push((shard.tenant_shard_id.tenant_id, guard));
+                }
+            }
+        }
+
+        // Process any deferred tenant drops
+        for (tenant_id, guard) in drop_detached_tenants {
+            self.maybe_drop_tenant(tenant_id, &mut locked, &guard);
         }
 
         metrics::METRICS_REGISTRY
diff --git a/storage_controller/src/tenant_shard.rs b/storage_controller/src/tenant_shard.rs
index cba579e8a749..c17989a316c7 100644
--- a/storage_controller/src/tenant_shard.rs
+++ b/storage_controller/src/tenant_shard.rs
@@ -465,6 +465,10 @@ impl ObservedState {
             locations: HashMap::new(),
         }
     }
+
+    pub(crate) fn is_empty(&self) -> bool {
+        self.locations.is_empty()
+    }
 }
 
 impl TenantShard {
diff --git a/test_runner/regress/test_storage_controller.py b/test_runner/regress/test_storage_controller.py
index 973d0cdf82cf..207f55a2144a 100644
--- a/test_runner/regress/test_storage_controller.py
+++ b/test_runner/regress/test_storage_controller.py
@@ -3299,13 +3299,116 @@ def test_storage_controller_detached_stopped(
             "generation": None,
         },
     )
-
+    env.storage_controller.reconcile_until_idle()
     env.storage_controller.consistency_check()
 
     # Confirm the detach happened
     assert env.pageserver.http_client().tenant_list_locations()["tenant_shards"] == []
 
 
+@run_only_on_default_postgres("Postgres version makes no difference here")
+def test_storage_controller_detach_lifecycle(
+    neon_env_builder: NeonEnvBuilder,
+):
+    """
+    Test that detached tenants are handled properly through their lifecycle: getting dropped
+    from memory when detached, then getting loaded back on-demand.
+    """
+
+    remote_storage_kind = s3_storage()
+    neon_env_builder.enable_pageserver_remote_storage(remote_storage_kind)
+
+    neon_env_builder.num_pageservers = 1
+
+    env = neon_env_builder.init_configs()
+    env.start()
+    virtual_ps_http = PageserverHttpClient(env.storage_controller_port, lambda: True)
+
+    tenant_id = TenantId.generate()
+    timeline_id = TimelineId.generate()
+    env.storage_controller.tenant_create(
+        tenant_id,
+        shard_count=1,
+    )
+    virtual_ps_http.timeline_create(PgVersion.NOT_SET, tenant_id, timeline_id)
+
+    remote_prefix = "/".join(
+        (
+            "tenants",
+            str(tenant_id),
+        )
+    )
+    # We will later check data is gone after deletion, so as a control check that it is present to begin with
+    assert_prefix_not_empty(
+        neon_env_builder.pageserver_remote_storage,
+        prefix=remote_prefix,
+    )
+
+    assert len(env.pageserver.http_client().tenant_list_locations()["tenant_shards"]) == 1
+    assert len(env.storage_controller.tenant_list()) == 1
+
+    # Detach the tenant
+    virtual_ps_http.tenant_location_conf(
+        tenant_id,
+        {
+            "mode": "Detached",
+            "secondary_conf": None,
+            "tenant_conf": {},
+            "generation": None,
+        },
+    )
+    # Ensure reconciles are done (the one we do inline in location_conf is advisory and if it takes too long that API just succeeds anyway)
+    env.storage_controller.reconcile_until_idle()
+    env.storage_controller.consistency_check()
+
+    # Confirm the detach happened on pageserver
+    assert env.pageserver.http_client().tenant_list_locations()["tenant_shards"] == []
+    # Confirm the tenant is not in memory on the controller
+    assert env.storage_controller.tenant_list() == []
+
+    # The detached tenant does not get loaded into memory across a controller restart
+    env.storage_controller.stop()
+    env.storage_controller.start()
+    assert env.storage_controller.tenant_list() == []
+    env.storage_controller.consistency_check()
+
+    # The detached tenant can be re-attached
+    virtual_ps_http.tenant_location_conf(
+        tenant_id,
+        {
+            "mode": "AttachedSingle",
+            "secondary_conf": None,
+            "tenant_conf": {},
+            "generation": None,
+        },
+    )
+    assert len(env.pageserver.http_client().tenant_list_locations()["tenant_shards"]) == 1
+    assert len(env.storage_controller.tenant_list()) == 1
+    env.storage_controller.consistency_check()
+
+    # Detach it again before doing deletion
+    virtual_ps_http.tenant_location_conf(
+        tenant_id,
+        {
+            "mode": "Detached",
+            "secondary_conf": None,
+            "tenant_conf": {},
+            "generation": None,
+        },
+    )
+    env.storage_controller.reconcile_until_idle()
+    env.storage_controller.consistency_check()
+
+    # A detached tenant can be deleted
+    virtual_ps_http.tenant_delete(tenant_id)
+
+    # Such deletions really work (empty remote storage)
+    assert_prefix_empty(
+        neon_env_builder.pageserver_remote_storage,
+        prefix=remote_prefix,
+    )
+
+
 @run_only_on_default_postgres("Postgres version makes no difference here")
 def test_storage_controller_node_flap_detach_race(
     neon_env_builder: NeonEnvBuilder,