diff --git a/include/i3.h b/include/i3.h
index f1912fd5..2a431486 100644
--- a/include/i3.h
+++ b/include/i3.h
@@ -37,6 +37,15 @@ extern bool debug_build;
 extern int listen_fds;
 extern xcb_connection_t *conn;
 extern int conn_screen;
+/**
+ * The EWMH support window that is used to indicate that an EWMH-compliant
+ * window manager is present. This window is created when i3 starts and
+ * kept alive until i3 exits.
+ * We also use this window as the focused window if no other window is
+ * available to be focused on the active workspace in order to prevent
+ * keyboard focus issues (see #1378).
+ */
+extern xcb_window_t ewmh_window;
 /** The last timestamp we got from X11 (timestamps are included in some events
  * and are used for some things, like determining a unique ID in startup
  * notification). */
diff --git a/src/ewmh.c b/src/ewmh.c
index 70cf7718..d60bbb50 100644
--- a/src/ewmh.c
+++ b/src/ewmh.c
@@ -11,6 +11,8 @@
  */
 #include "all.h"
 
+xcb_window_t ewmh_window;
+
 /*
  * Updates _NET_CURRENT_DESKTOP with the current desktop number.
  *
@@ -227,25 +229,30 @@ void ewmh_setup_hints(void) {
      * present, a child window has to be created (and kept alive as long as the
      * window manager is running) which has the _NET_SUPPORTING_WM_CHECK and
      * _NET_WM_ATOMS. */
-    xcb_window_t child_window = xcb_generate_id(conn);
+    ewmh_window = xcb_generate_id(conn);
+    /* We create the window and put it at (-1, -1) so that it is off-screen. */
     xcb_create_window(
         conn,
         XCB_COPY_FROM_PARENT,        /* depth */
-        child_window,                /* window id */
+        ewmh_window,                 /* window id */
         root,                        /* parent */
-        0, 0, 1, 1,                  /* dimensions (x, y, w, h) */
+        -1, -1, 1, 1,                /* dimensions (x, y, w, h) */
         0,                           /* border */
         XCB_WINDOW_CLASS_INPUT_ONLY, /* window class */
         XCB_COPY_FROM_PARENT,        /* visual */
-        0,
-        NULL);
-    xcb_change_property(conn, XCB_PROP_MODE_REPLACE, child_window, A__NET_SUPPORTING_WM_CHECK, XCB_ATOM_WINDOW, 32, 1, &child_window);
-    xcb_change_property(conn, XCB_PROP_MODE_REPLACE, child_window, A__NET_WM_NAME, A_UTF8_STRING, 8, strlen("i3"), "i3");
-    xcb_change_property(conn, XCB_PROP_MODE_REPLACE, root, A__NET_SUPPORTING_WM_CHECK, XCB_ATOM_WINDOW, 32, 1, &child_window);
+        XCB_CW_OVERRIDE_REDIRECT,
+        (uint32_t[]){1});
+    xcb_change_property(conn, XCB_PROP_MODE_REPLACE, ewmh_window, A__NET_SUPPORTING_WM_CHECK, XCB_ATOM_WINDOW, 32, 1, &ewmh_window);
+    xcb_change_property(conn, XCB_PROP_MODE_REPLACE, ewmh_window, A__NET_WM_NAME, A_UTF8_STRING, 8, strlen("i3"), "i3");
+    xcb_change_property(conn, XCB_PROP_MODE_REPLACE, root, A__NET_SUPPORTING_WM_CHECK, XCB_ATOM_WINDOW, 32, 1, &ewmh_window);
 
     /* I’m not entirely sure if we need to keep _NET_WM_NAME on root. */
     xcb_change_property(conn, XCB_PROP_MODE_REPLACE, root, A__NET_WM_NAME, A_UTF8_STRING, 8, strlen("i3"), "i3");
 
     /* only send the first 31 atoms (last one is _NET_CLOSE_WINDOW) increment that number when adding supported atoms */
     xcb_change_property(conn, XCB_PROP_MODE_REPLACE, root, A__NET_SUPPORTED, XCB_ATOM_ATOM, 32, /* number of atoms */ 31, supported_atoms);
+
+    /* We need to map this window to be able to set the input focus to it if no other window is available to be focused. */
+    xcb_map_window(conn, ewmh_window);
+    xcb_configure_window(conn, ewmh_window, XCB_CONFIG_WINDOW_STACK_MODE, (uint32_t[]){XCB_STACK_MODE_BELOW});
 }
diff --git a/src/x.c b/src/x.c
index 337e268c..f0da9fff 100644
--- a/src/x.c
+++ b/src/x.c
@@ -12,6 +12,8 @@
  */
 #include "all.h"
 
+xcb_window_t ewmh_window;
+
 /* Stores the X11 window ID of the currently focused window */
 xcb_window_t focused_id = XCB_NONE;
 
@@ -1090,10 +1092,12 @@ void x_push_changes(Con *con) {
     }
 
     if (focused_id == XCB_NONE) {
-        DLOG("Still no window focused, better set focus to the root window\n");
-        xcb_set_input_focus(conn, XCB_INPUT_FOCUS_POINTER_ROOT, root, XCB_CURRENT_TIME);
+        /* If we still have no window to focus, we focus the EWMH window instead. We use this rather than the
+         * root window in order to avoid an X11 fallback mechanism causing a ghosting effect (see #1378). */
+        DLOG("Still no window focused, better set focus to the EWMH support window (%d)\n", ewmh_window);
+        xcb_set_input_focus(conn, XCB_INPUT_FOCUS_POINTER_ROOT, ewmh_window, XCB_CURRENT_TIME);
         ewmh_update_active_window(XCB_WINDOW_NONE);
-        focused_id = root;
+        focused_id = ewmh_window;
     }
 
     xcb_flush(conn);
diff --git a/testcases/t/527-focus-fallback.t b/testcases/t/527-focus-fallback.t
new file mode 100644
index 00000000..5956e67f
--- /dev/null
+++ b/testcases/t/527-focus-fallback.t
@@ -0,0 +1,45 @@
+#!perl
+# vim:ts=4:sw=4:expandtab
+#
+# Please read the following documents before working on tests:
+# • http://build.i3wm.org/docs/testsuite.html
+#   (or docs/testsuite)
+#
+# • http://build.i3wm.org/docs/lib-i3test.html
+#   (alternatively: perldoc ./testcases/lib/i3test.pm)
+#
+# • http://build.i3wm.org/docs/ipc.html
+#   (or docs/ipc)
+#
+# • http://onyxneon.com/books/modern_perl/modern_perl_a4.pdf
+#   (unless you are already familiar with Perl)
+#
+# Ticket: #1378
+use i3test;
+use X11::XCB qw(:all);
+
+sub get_ewmh_window {
+    my $cookie = $x->get_property(
+        0,
+        $x->get_root_window(),
+        $x->atom(name => '_NET_SUPPORTING_WM_CHECK')->id,
+        $x->atom(name => 'WINDOW')->id,
+        0,
+        4096
+    );
+
+    my $reply = $x->get_property_reply($cookie->{sequence});
+    my $len = $reply->{length};
+    return undef if $len == 0;
+
+    return unpack("L", $reply->{value});
+}
+
+my $window = open_window;
+sync_with_i3;
+is($x->input_focus, $window->id, 'sanity check: window has input focus');
+cmd 'kill';
+sync_with_i3;
+is($x->input_focus, get_ewmh_window(), 'focus falls back to the EWMH window');
+
+done_testing;