diff --git a/db/hints/manager.cc b/db/hints/manager.cc
index 74d00593f9..9c24d668dd 100644
--- a/db/hints/manager.cc
+++ b/db/hints/manager.cc
@@ -547,10 +547,16 @@ future<> manager::change_host_filter(host_filter filter) {
             const auto maybe_host_id_and_ip = std::invoke([&] () -> std::optional<pair_type> {
                 try {
                     locator::host_id_or_endpoint hid_or_ep{de.name};
-                    if (hid_or_ep.has_host_id()) {
+
+                    // If hinted handoff is host-ID-based, hint directories representing IP addresses must've
+                    // been created by mistake and they're invalid. The same for pre-host-ID hinted handoff
+                    // -- hint directories representing host IDs are NOT valid.
+                    if (hid_or_ep.has_host_id() && _uses_host_id) {
                         return std::make_optional(pair_type{hid_or_ep.id(), hid_or_ep.resolve_endpoint(*tmptr)});
-                    } else {
+                    } else if (hid_or_ep.has_endpoint() && !_uses_host_id) {
                         return std::make_optional(pair_type{hid_or_ep.resolve_id(*tmptr), hid_or_ep.endpoint()});
+                    } else {
+                        return std::nullopt;
                     }
                 } catch (...) {
                     return std::nullopt;
@@ -712,8 +718,6 @@ future<> manager::with_file_update_mutex_for(const std::variant<locator::host_id
     return _ep_managers.at(host_id).with_file_update_mutex(std::move(func));
 }
 
-// The function assumes that if `_uses_host_id == true`, then there are no directories that represent IP addresses,
-// i.e. every directory is either valid and represents a host ID, or is invalid (so it should be ignored anyway).
 future<> manager::initialize_endpoint_managers() {
     auto maybe_create_ep_mgr = [this] (const locator::host_id& host_id, const gms::inet_address& ip) -> future<> {
         if (!check_dc_for(host_id)) {
@@ -747,12 +751,23 @@ future<> manager::initialize_endpoint_managers() {
         }
 
         if (_uses_host_id) {
+            // If hinted handoff is host-ID-based but the directory doesn't represent a host ID,
+            // it's invalid. Ignore it.
+            if (!maybe_host_id_or_ep->has_host_id()) {
+                co_return;
+            }
+
             // If hinted handoff is host-ID-based, `get_ep_manager` will NOT use the passed IP address,
             // so we simply pass the default value there.
             co_return co_await maybe_create_ep_mgr(maybe_host_id_or_ep->id(), gms::inet_address{});
         }
 
         // If we have got to this line, hinted handoff is still IP-based and we need to map the IP.
+        if (!maybe_host_id_or_ep->has_endpoint()) {
+            // If the directory name doesn't represent an IP, it's invalid. We ignore it.
+            co_return;
+        }
+
         const auto maybe_host_id = std::invoke([&] () -> std::optional<locator::host_id> {
             try {
                 return maybe_host_id_or_ep->resolve_id(*tmptr);
diff --git a/db/hints/manager.hh b/db/hints/manager.hh
index b2a9a5bfc6..64041c2601 100644
--- a/db/hints/manager.hh
+++ b/db/hints/manager.hh
@@ -323,6 +323,10 @@ public:
 
     void update_backlog(size_t backlog, size_t max_backlog);
 
+    bool uses_host_id() const noexcept {
+        return _uses_host_id;
+    }
+
 private:
     bool stopping() const noexcept {
         return _state.contains(state::stopping);
diff --git a/db/hints/resource_manager.cc b/db/hints/resource_manager.cc
index 00b2b439eb..ceae530c71 100644
--- a/db/hints/resource_manager.cc
+++ b/db/hints/resource_manager.cc
@@ -148,10 +148,16 @@ void space_watchdog::on_timer() {
                 auto maybe_variant = std::invoke([&] () -> std::optional<std::variant<locator::host_id, gms::inet_address>> {
                     try {
                         const auto hid_or_ep = locator::host_id_or_endpoint{de.name};
-                        if (hid_or_ep.has_host_id()) {
+
+                        // If hinted handoff is host-ID-based, hint directories representing IP addresses must've
+                        // been created by mistake and they're invalid. The same for pre-host-ID hinted handoff
+                        // -- hint directories representing host IDs are NOT valid.
+                        if (hid_or_ep.has_host_id() && shard_manager.uses_host_id()) {
                             return std::variant<locator::host_id, gms::inet_address>(hid_or_ep.id());
-                        } else {
+                        } else if (hid_or_ep.has_endpoint() && !shard_manager.uses_host_id()) {
                             return std::variant<locator::host_id, gms::inet_address>(hid_or_ep.endpoint());
+                        } else {
+                            return std::nullopt;
                         }
                     } catch (...) {
                         return std::nullopt;