diff --git a/src/lib_shell/block_validator.ml b/src/lib_shell/block_validator.ml
index 0cff97e7526fdc6509b72a29c4cb317645074a68..3485999e40c9c39180bfa3cb4e8badf81f11371c 100644
--- a/src/lib_shell/block_validator.ml
+++ b/src/lib_shell/block_validator.ml
@@ -412,6 +412,26 @@ let on_error (type a b) (_w : t) st (r : (a, b) Request.t) (errs : b) =
       (* Keep the worker alive. *)
       return_ok_unit
 
+(* This failsafe aims to look for an irmin error that is known to be
+   critical and, if found, stop the node gracefully. *)
+let check_and_quit_on_irmin_errors errors =
+  let open Lwt_syntax in
+  let is_inode_error error =
+    match error with
+    | Exn (Failure s) -> (
+        let rex = Str.regexp_string "unknown inode key" in
+        try
+          let _ = Str.search_forward rex s 0 in
+          true
+        with Not_found -> false)
+    | _ -> false
+  in
+  if List.exists (fun error -> is_inode_error error) errors then
+    let* () = Events.(emit stopping_node_missing_irmin_key ()) in
+    let* _ = Lwt_exit.exit_and_wait 1 in
+    return_unit
+  else return_unit
+
 let on_completion :
     type a b.
     t -> (a, b) Request.t -> a -> Worker_types.request_status -> unit Lwt.t =
@@ -442,7 +462,10 @@ let on_completion :
           | [Canceled] ->
               (* Ignore requests cancellation *)
               Lwt.return_unit
-          | errs -> Events.(emit validation_failure) (v.block, st, errs))
+          | errs ->
+              let* () = Events.(emit validation_failure) (v.block, st, errs) in
+              let* () = check_and_quit_on_irmin_errors errs in
+              return_unit)
       | _ -> (* assert false *) Lwt.return_unit)
   | Request.Request_preapplication _, Preapplied _ -> (
       Prometheus.Counter.inc_one metrics.preapplied_blocks_count ;
@@ -453,14 +476,20 @@ let on_completion :
       Prometheus.Counter.inc_one metrics.preapplication_errors_count ;
       match Request.view request with
       | Preapplication v ->
-          Events.(emit preapplication_failure) (v.level, st, errs)
+          let* () = Events.(emit preapplication_failure) (v.level, st, errs) in
+          let* () = check_and_quit_on_irmin_errors errs in
+          return_unit
       | _ -> (* assert false *) Lwt.return_unit)
   | Request.Request_validation _, Validation_error_after_precheck errs -> (
       Shell_metrics.Worker.update_timestamps metrics.worker_timestamps st ;
       Prometheus.Counter.inc_one metrics.validation_errors_after_precheck_count ;
       match Request.view request with
       | Validation v ->
-          Events.(emit validation_failure_after_precheck) (v.block, st, errs)
+          let* () =
+            Events.(emit validation_failure_after_precheck) (v.block, st, errs)
+          in
+          let* () = check_and_quit_on_irmin_errors errs in
+          return_unit
       | _ -> (* assert false *) Lwt.return_unit)
   | Request.Request_validation _, Precheck_failed errs -> (
       Shell_metrics.Worker.update_timestamps metrics.worker_timestamps st ;
@@ -471,7 +500,10 @@ let on_completion :
           | [Canceled] ->
               (* Ignore requests cancellation *)
               Lwt.return_unit
-          | errs -> Events.(emit precheck_failure) (v.block, st, errs))
+          | errs ->
+              let* () = Events.(emit precheck_failure) (v.block, st, errs) in
+              let* () = check_and_quit_on_irmin_errors errs in
+              return_unit)
       | _ -> (* assert false *) Lwt.return_unit)
   | _ -> (* assert false *) Lwt.return_unit
 
diff --git a/src/lib_shell/block_validator_events.ml b/src/lib_shell/block_validator_events.ml
index 6876c8006b620e7f6ac76b576a50f46d38cb7143..ac61cbb92a8bf08ef352249c552ce8a5e89849ad 100644
--- a/src/lib_shell/block_validator_events.ml
+++ b/src/lib_shell/block_validator_events.ml
@@ -149,3 +149,11 @@ let could_not_find_context =
     ~msg:"could not find context for block {hash}"
     ~pp1:Block_hash.pp
     ("hash", Block_hash.encoding)
+
+let stopping_node_missing_irmin_key =
+  declare_0
+    ~section
+    ~name:"stopping_node_missing_irmin_key"
+    ~level:Error
+    ~msg:"critical irmin error: stopping the node gracefully."
+    ()