diff --git a/src/mito2/src/error.rs b/src/mito2/src/error.rs
index 74ea47b653..86b310e1ac 100644
--- a/src/mito2/src/error.rs
+++ b/src/mito2/src/error.rs
@@ -490,6 +490,18 @@ pub enum Error {
         location: Location,
     },
 
+    #[snafu(display(
+        "Region {} is in {:?} state, which does not permit manifest updates.",
+        region_id,
+        state
+    ))]
+    UpdateManifest {
+        region_id: RegionId,
+        state: RegionRoleState,
+        #[snafu(implicit)]
+        location: Location,
+    },
+
     #[snafu(display("Region {} is in {:?} state, expect: {:?}", region_id, state, expect))]
     RegionLeaderState {
         region_id: RegionId,
@@ -1055,7 +1067,7 @@ impl ErrorExt for Error {
             CompactRegion { source, .. } => source.status_code(),
             CompatReader { .. } => StatusCode::Unexpected,
             InvalidRegionRequest { source, .. } => source.status_code(),
-            RegionLeaderState { .. } => StatusCode::RegionNotReady,
+            RegionLeaderState { .. } | UpdateManifest { .. } => StatusCode::RegionNotReady,
             &FlushableRegionState { .. } => StatusCode::RegionNotReady,
             JsonOptions { .. } => StatusCode::InvalidArguments,
             EmptyRegionDir { .. } | EmptyManifestDir { .. } => StatusCode::RegionNotFound,
diff --git a/src/mito2/src/region.rs b/src/mito2/src/region.rs
index 90d2f55e5e..4a5beb0cb5 100644
--- a/src/mito2/src/region.rs
+++ b/src/mito2/src/region.rs
@@ -36,7 +36,7 @@ use store_api::storage::RegionId;
 use crate::access_layer::AccessLayerRef;
 use crate::error::{
     FlushableRegionStateSnafu, RegionLeaderStateSnafu, RegionNotFoundSnafu, RegionTruncatedSnafu,
-    Result,
+    Result, UpdateManifestSnafu,
 };
 use crate::manifest::action::{RegionMetaAction, RegionMetaActionList};
 use crate::manifest::manager::RegionManifestManager;
@@ -371,14 +371,36 @@ impl ManifestContext {
         // Checks state inside the lock. This is to ensure that we won't update the manifest
         // after `set_readonly_gracefully()` is called.
         let current_state = self.state.load();
-        ensure!(
-            current_state == RegionRoleState::Leader(expect_state),
-            RegionLeaderStateSnafu {
-                region_id: manifest.metadata.region_id,
-                state: current_state,
-                expect: expect_state,
+
+        // If expect_state is not downgrading, the current state must be either `expect_state` or downgrading.
+        //
+        // A downgrading leader rejects user writes but still allows
+        // flushing the memtable and updating the manifest.
+        if expect_state != RegionLeaderState::Downgrading {
+            if current_state == RegionRoleState::Leader(RegionLeaderState::Downgrading) {
+                info!(
+                    "Region {} is in downgrading leader state, updating manifest. state is {:?}",
+                    manifest.metadata.region_id, expect_state
+                );
             }
-        );
+            ensure!(
+                current_state == RegionRoleState::Leader(expect_state)
+                    || current_state == RegionRoleState::Leader(RegionLeaderState::Downgrading),
+                UpdateManifestSnafu {
+                    region_id: manifest.metadata.region_id,
+                    state: current_state,
+                }
+            );
+        } else {
+            ensure!(
+                current_state == RegionRoleState::Leader(expect_state),
+                RegionLeaderStateSnafu {
+                    region_id: manifest.metadata.region_id,
+                    state: current_state,
+                    expect: expect_state,
+                }
+            );
+        }
 
         for action in &action_list.actions {
             // Checks whether the edit is still applicable.