diff --git a/pageserver/src/tenant/secondary/heatmap_uploader.rs b/pageserver/src/tenant/secondary/heatmap_uploader.rs
index c5e5e04945..d72c337369 100644
--- a/pageserver/src/tenant/secondary/heatmap_uploader.rs
+++ b/pageserver/src/tenant/secondary/heatmap_uploader.rs
@@ -9,13 +9,14 @@ use crate::{
     metrics::SECONDARY_MODE,
     tenant::{
         config::AttachmentMode,
-        mgr::GetTenantError,
-        mgr::TenantManager,
+        mgr::{GetTenantError, TenantManager},
         remote_timeline_client::remote_heatmap_path,
         span::debug_assert_current_span_has_tenant_id,
         tasks::{warn_when_period_overrun, BackgroundLoopKind},
         Tenant,
     },
+    virtual_file::VirtualFile,
+    TEMP_FILE_SUFFIX,
 };
 
 use futures::Future;
@@ -32,7 +33,10 @@ use super::{
 };
 use tokio_util::sync::CancellationToken;
 use tracing::{info_span, instrument, Instrument};
-use utils::{backoff, completion::Barrier, yielding_loop::yielding_loop};
+use utils::{
+    backoff, completion::Barrier, crashsafe::path_with_suffix_extension,
+    yielding_loop::yielding_loop,
+};
 
 pub(super) async fn heatmap_uploader_task(
     tenant_manager: Arc<TenantManager>,
@@ -461,6 +465,18 @@ async fn upload_tenant_heatmap(
         }
     }
 
+    // After a successful upload persist the fresh heatmap to disk.
+    // When restarting, the tenant will read the heatmap from disk
+    // and additively generate a new heatmap (see [`Timeline::generate_heatmap`]).
+    // If the heatmap is stale, the additive generation can lead to keeping previously
+    // evicted timelines on the secondarie's disk.
+    let tenant_shard_id = tenant.get_tenant_shard_id();
+    let heatmap_path = tenant.conf.tenant_heatmap_path(tenant_shard_id);
+    let temp_path = path_with_suffix_extension(&heatmap_path, TEMP_FILE_SUFFIX);
+    if let Err(err) = VirtualFile::crashsafe_overwrite(heatmap_path, temp_path, bytes).await {
+        tracing::warn!("Non fatal IO error writing to disk after heatmap upload: {err}");
+    }
+
     tracing::info!("Successfully uploaded {size} byte heatmap to {path}");
 
     Ok(UploadHeatmapOutcome::Uploaded(LastUploadState {
diff --git a/test_runner/fixtures/neon_fixtures.py b/test_runner/fixtures/neon_fixtures.py
index 8909f7f249..7c4991ffab 100644
--- a/test_runner/fixtures/neon_fixtures.py
+++ b/test_runner/fixtures/neon_fixtures.py
@@ -2766,6 +2766,11 @@ class NeonPageserver(PgProtocol, LogUtils):
             log.error(f"Failed to decode LocationConf, raw content ({len(bytes)} bytes): {bytes}")
             raise
 
+    def heatmap_content(self, tenant_shard_id: TenantId | TenantShardId) -> Any:
+        path = self.tenant_dir(tenant_shard_id) / "heatmap-v1.json"
+        with open(path) as f:
+            return json.load(f)
+
     def tenant_create(
         self,
         tenant_id: TenantId,
diff --git a/test_runner/regress/test_pageserver_secondary.py b/test_runner/regress/test_pageserver_secondary.py
index 1292682f9e..590093d23c 100644
--- a/test_runner/regress/test_pageserver_secondary.py
+++ b/test_runner/regress/test_pageserver_secondary.py
@@ -443,7 +443,7 @@ def test_heatmap_uploads(neon_env_builder: NeonEnvBuilder):
     workload.write_rows(256, env.pageservers[0].id)
     env.pageserver.http_client().tenant_heatmap_upload(tenant_id)
 
-    def validate_heatmap(heatmap):
+    def validate_heatmap(heatmap, on_disk_heatmap):
         assert len(heatmap["timelines"]) == 1
         assert heatmap["timelines"][0]["timeline_id"] == str(timeline_id)
         assert len(heatmap["timelines"][0]["layers"]) > 0
@@ -452,10 +452,13 @@ def test_heatmap_uploads(neon_env_builder: NeonEnvBuilder):
         # Each layer appears at most once
         assert len(set(layer["name"] for layer in layers)) == len(layers)
 
+        assert heatmap == on_disk_heatmap
+
     # Download and inspect the heatmap that the pageserver uploaded
     heatmap_first = env.pageserver_remote_storage.heatmap_content(tenant_id)
+    heatmap_first_on_disk = env.pageserver.heatmap_content(tenant_id)
     log.info(f"Read back heatmap: {heatmap_first}")
-    validate_heatmap(heatmap_first)
+    validate_heatmap(heatmap_first, heatmap_first_on_disk)
 
     # Do some more I/O to generate more layers
     workload.churn_rows(64, env.pageservers[0].id)
@@ -463,9 +466,10 @@ def test_heatmap_uploads(neon_env_builder: NeonEnvBuilder):
 
     # Ensure that another heatmap upload includes the new layers
     heatmap_second = env.pageserver_remote_storage.heatmap_content(tenant_id)
+    heatmap_second_on_disk = env.pageserver.heatmap_content(tenant_id)
     log.info(f"Read back heatmap: {heatmap_second}")
     assert heatmap_second != heatmap_first
-    validate_heatmap(heatmap_second)
+    validate_heatmap(heatmap_second, heatmap_second_on_disk)
 
 
 def list_elegible_layers(