diff --git a/src/86box.c b/src/86box.c
index db0182d84..4eae7ab02 100644
--- a/src/86box.c
+++ b/src/86box.c
@@ -32,6 +32,7 @@
 
 #ifndef _WIN32
 #include <pwd.h>
+#include <unistd.h>
 #endif
 #ifdef __APPLE__
 #include <string.h>
@@ -125,6 +126,7 @@ uint64_t	unique_id = 0;
 uint64_t	source_hwnd = 0;
 #endif
 char	rom_path[1024] = { '\0'};		/* (O) full path to ROMs */
+rom_path_t rom_paths = { "", NULL };    /* (O) full paths to ROMs */
 char	log_path[1024] = { '\0'};		/* (O) full path of logfile */
 char	vm_name[1024]  = { '\0'};		/* (O) display name of the VM */
 
@@ -383,6 +385,48 @@ pc_log(const char *fmt, ...)
 #define pc_log(fmt, ...)
 #endif
 
+void
+add_rom_path(const char* path)
+{
+    static char cwd[1024];
+    memset(cwd, 0x00, sizeof(cwd));
+    rom_path_t* cur_rom_path = &rom_paths;
+    while (cur_rom_path->next != NULL) {
+        cur_rom_path = cur_rom_path->next;
+    }
+    if (!plat_path_abs((char*)path)) {
+        /*
+         * This looks like a relative path.
+         *
+         * Add it to the current working directory
+         * to convert it (back) to an absolute path.
+         */
+        plat_getcwd(cwd, 1024);
+        plat_path_slash(cwd);
+        snprintf(cur_rom_path->rom_path, 1024, "%s%s%c", cwd, path, 0);
+    }
+    else {
+        /*
+         * The user-provided path seems like an
+         * absolute path, so just use that.
+         */
+        strncpy(cur_rom_path->rom_path, path, 1024);
+    }
+    plat_path_slash(cur_rom_path->rom_path);
+    cur_rom_path->next = calloc(1, sizeof(rom_path_t));
+}
+
+// Copied over from Unix code, which in turn is lifted from musl. Needed for parsing XDG_DATA_DIRS.
+static char *local_strsep(char **str, const char *sep)
+{
+    char *s = *str, *end;
+    if (!s) return NULL;
+    end = s + strcspn(s, sep);
+    if (*end) *end++ = 0;
+    else end = 0;
+    *str = end;
+    return s;
+}
 
 /*
  * Perform initial startup of the PC.
@@ -496,6 +540,7 @@ usage:
 			if ((c+1) == argc) goto usage;
 
 			strcpy(path2, argv[++c]);
+            add_rom_path(path2);
 		} else if (!strcasecmp(argv[c], "--config") ||
 			   !strcasecmp(argv[c], "-C")) {
 			if ((c+1) == argc) goto usage;
@@ -591,26 +636,44 @@ usage:
 			plat_dir_create(usr_path);
 	}
 
-	if (path2[0] == '\0') {
+    if (vmrp) {
+        char vmrppath[1024] = { 0 };
+        strcpy(vmrppath, usr_path);
+        plat_path_slash(vmrppath);
+        strcat(vmrppath, "roms");
+        plat_path_slash(vmrppath);
+        add_rom_path(vmrppath);
+        if (path2[0] == '\0') {
+            strcpy(path2, vmrppath);
+        }
+    }
+
+    {
+        char default_rom_path[1024] = { 0 };
 #if defined(__APPLE__)
-		getDefaultROMPath(path2);
+        getDefaultROMPath(default_rom_path);
 #elif !defined(_WIN32)
 		appimage = getenv("APPIMAGE");
 		if (appimage && (appimage[0] != '\0')) {
-			plat_get_dirname(path2, appimage);
-			plat_path_slash(path2);
-			strcat(path2, "roms");
-			plat_path_slash(path2);
+            plat_get_dirname(default_rom_path, appimage);
+            plat_path_slash(default_rom_path);
+            strcat(default_rom_path, "roms");
+            plat_path_slash(default_rom_path);
 		}
 #endif
+        if (default_rom_path[0] == '\0') {
+            plat_getcwd(default_rom_path, 1024);
+            plat_path_slash(default_rom_path);
+            snprintf(default_rom_path, 1024, "%s%s%c", default_rom_path, "roms", 0);
+            plat_path_slash(default_rom_path);
+        }
+        add_rom_path(default_rom_path);
+        if (path2[0] == '\0') {
+            strcpy(path2, default_rom_path);
+        }
 	}
 
-	if (vmrp && (path2[0] == '\0')) {
-		strcpy(path2, usr_path);
-		plat_path_slash(path2);
-		strcat(path2, "roms");
-		plat_path_slash(path2);
-	}
+    plat_init_rom_paths();
 
 	/*
 	 * If the user provided a path for ROMs, use that
@@ -708,8 +771,13 @@ usage:
 	pclog("# VM: %s\n#\n", vm_name);
 	pclog("# Emulator path: %s\n", exe_path);
 	pclog("# Userfiles path: %s\n", usr_path);
-	if (rom_path[0] != '\0')
-		pclog("# ROM path: %s\n", rom_path);
+    if (rom_paths.next) {
+        rom_path_t* cur_rom_path = &rom_paths;
+        while (cur_rom_path->next) {
+            pclog("# ROM path: %s\n", cur_rom_path->rom_path);
+            cur_rom_path = cur_rom_path->next;
+        }
+    }
 	else
 #ifndef _WIN32
 	pclog("# ROM path: %sroms/\n", exe_path);
diff --git a/src/include/86box/plat.h b/src/include/86box/plat.h
index 71ad89927..ad7006165 100644
--- a/src/include/86box/plat.h
+++ b/src/include/86box/plat.h
@@ -104,6 +104,7 @@ extern int	plat_getcwd(char *bufp, int max);
 extern int	plat_chdir(char *path);
 extern void	plat_tempfile(char *bufp, char *prefix, char *suffix);
 extern void	plat_get_exe_name(char *s, int size);
+extern void plat_init_rom_paths();
 extern char	*plat_get_basename(const char *path);
 extern void	plat_get_dirname(char *dest, const char *path);
 extern char	*plat_get_filename(char *s);
diff --git a/src/include/86box/rom.h b/src/include/86box/rom.h
index dfea9f0b5..04fe94422 100644
--- a/src/include/86box/rom.h
+++ b/src/include/86box/rom.h
@@ -41,6 +41,15 @@ typedef struct {
 } rom_t;
 
 
+typedef struct rom_path_t {
+    char rom_path[1024];
+    struct rom_path_t* next;
+} rom_path_t;
+
+extern rom_path_t rom_paths;
+
+extern void add_rom_path(const char* path);
+
 extern uint8_t	rom_read(uint32_t addr, void *p);
 extern uint16_t	rom_readw(uint32_t addr, void *p);
 extern uint32_t	rom_readl(uint32_t addr, void *p);
diff --git a/src/mem/rom.c b/src/mem/rom.c
index 30e873a4e..3dcbfe568 100644
--- a/src/mem/rom.c
+++ b/src/mem/rom.c
@@ -69,11 +69,19 @@ rom_fopen(char *fn, char *mode)
 	fn2 = (char *) malloc(strlen(fn) + 1);
 	memcpy(fn2, fn, strlen(fn) + 1);
 
-	if (rom_path[0] != '\0') {
+    if (rom_paths.next) {
+        rom_path_t* cur_rom_path = &rom_paths;
 		memset(fn2, 0x00, strlen(fn) + 1);
 		memcpy(fn2, &(fn[5]), strlen(fn) - 4);
 
-		plat_append_filename(temp, rom_path, fn2);
+        while (cur_rom_path->next) {
+            memset(temp, 0, sizeof(temp));
+            plat_append_filename(temp, cur_rom_path->rom_path, fn2);
+            if (rom_present(temp)) {
+                break;
+            }
+            cur_rom_path = cur_rom_path->next;
+        }
 	} else {
 		/* Make sure to make it a backslash, just in case there's malformed
 		   code calling us that assumes Windows. */
@@ -97,17 +105,54 @@ rom_fopen(char *fn, char *mode)
 int
 rom_getfile(char *fn, char *s, int size)
 {
-    FILE *f;
+    char temp[1024] = {'\0'};
+    char *fn2;
+    int retval = 0;
 
-    plat_append_filename(s, exe_path, fn);
+    if ((strstr(fn, "roms/") == fn) || (strstr(fn, "roms\\") == fn)) {
+    /* Relative path */
+    fn2 = (char *) malloc(strlen(fn) + 1);
+    memcpy(fn2, fn, strlen(fn) + 1);
 
-    f = plat_fopen(s, "rb");
-    if (f != NULL) {
-	(void)fclose(f);
-	return(1);
+    if (rom_paths.next) {
+        rom_path_t* cur_rom_path = &rom_paths;
+        memset(fn2, 0x00, strlen(fn) + 1);
+        memcpy(fn2, &(fn[5]), strlen(fn) - 4);
+
+        while (cur_rom_path->next) {
+            memset(temp, 0, sizeof(temp));
+            plat_append_filename(temp, cur_rom_path->rom_path, fn2);
+            if (rom_present(temp)) {
+                strncpy(s, temp, size);
+                retval = 1;
+                break;
+            }
+            cur_rom_path = cur_rom_path->next;
+        }
+    } else {
+        /* Make sure to make it a backslash, just in case there's malformed
+           code calling us that assumes Windows. */
+        if (fn2[4] == '\\')
+            fn2[4] = '/';
+
+        plat_append_filename(temp, exe_path, fn2);
+        if (rom_present(temp)) {
+            strncpy(s, temp, size);
+            retval = 1;
+        }
     }
 
-    return(0);
+    free(fn2);
+    fn2 = NULL;
+    } else {
+        /* Absolute path */
+        if (rom_present(fn)) {
+            strncpy(s, fn, size);
+            retval = 1;
+        }
+    }
+
+    return(retval);
 }
 
 
diff --git a/src/qt/qt_platform.cpp b/src/qt/qt_platform.cpp
index ff7b99c93..e6e3256d3 100644
--- a/src/qt/qt_platform.cpp
+++ b/src/qt/qt_platform.cpp
@@ -88,6 +88,8 @@ extern "C" {
 #include <86box/timer.h>
 #include <86box/nvr.h>
 #include <86box/plat_dynld.h>
+#include <86box/mem.h>
+#include <86box/rom.h>
 #include <86box/config.h>
 #include <86box/ui.h>
 #include <86box/discord.h>
@@ -583,3 +585,63 @@ plat_chdir(char *path)
 {
     return QDir::setCurrent(QString(path)) ? 0 : -1;
 }
+
+void
+plat_init_rom_paths()
+{
+#if defined __APPLE__
+    QDir::root().mkpath(QStringLiteral("%1/Documents/86Box/roms/").arg(QDir::homePath()));
+    add_rom_path(QStringLiteral("%1/Documents/86Box/roms/").arg(QDir::homePath()).toUtf8().constData());
+#elif !defined _WIN32
+    if (getenv("XDG_DATA_HOME")) {
+        char xdg_rom_path[1024 + 1] = { 0 };
+        strncpy(xdg_rom_path, getenv("XDG_DATA_HOME"), 1024);
+        plat_path_slash(xdg_rom_path);
+        strncat(xdg_rom_path, "86Box/", 1024);
+
+        if (!plat_dir_check(xdg_rom_path))
+            plat_dir_create(xdg_rom_path);
+        strcat(xdg_rom_path, "roms/");
+
+        if (!plat_dir_check(xdg_rom_path))
+            plat_dir_create(xdg_rom_path);
+        add_rom_path(xdg_rom_path);
+    } else {
+        char home_rom_path[1024] = { 0 };
+        snprintf(home_rom_path, 1024, "%s/.local/share/86Box/", getenv("HOME") ? getenv("HOME") : QDir::homePath().toUtf8().constData());
+
+        if (!plat_dir_check(home_rom_path))
+            plat_dir_create(home_rom_path);
+        strcat(home_rom_path, "roms/");
+
+        if (!plat_dir_check(home_rom_path))
+            plat_dir_create(home_rom_path);
+        add_rom_path(home_rom_path);
+    }
+    if (getenv("XDG_DATA_DIRS")) {
+        char* xdg_rom_paths = strdup(getenv("XDG_DATA_DIRS"));
+        char* xdg_rom_paths_orig = xdg_rom_paths;
+        char* cur_xdg_rom_path = NULL;
+        if (xdg_rom_paths) {
+            while (xdg_rom_paths[strlen(xdg_rom_paths) - 1] == ':') {
+                xdg_rom_paths[strlen(xdg_rom_paths) - 1] = '\0';
+            }
+            QStringList path_list = QString(xdg_rom_paths).split(":");
+            for (auto& cur_path : path_list) {
+                if (cur_path.right(1) != '/')
+                    cur_path.push_back('/');
+                add_rom_path((cur_path + "86Box/roms").toUtf8().constData());
+            }
+        }
+        free(xdg_rom_paths_orig);
+    } else {
+        add_rom_path("/usr/local/share/86Box/roms/");
+        add_rom_path("/usr/share/86Box/roms/");
+    }
+#elif _WIN32
+    auto appDataDir = QDir(qEnvironmentVariable("LOCALAPPDATA"));
+    appDataDir.mkdir("86Box");
+    appDataDir.mkdir("86Box/roms");
+    add_rom_path((appDataDir.path().replace("\\","/") + "/86Box/roms").toUtf8().constData());
+#endif
+}
diff --git a/src/unix/unix.c b/src/unix/unix.c
index 1f60ad565..5f6429b89 100644
--- a/src/unix/unix.c
+++ b/src/unix/unix.c
@@ -21,6 +21,8 @@
 #include <stdatomic.h>
 
 #include <86box/86box.h>
+#include <86box/mem.h>
+#include <86box/rom.h>
 #include <86box/keyboard.h>
 #include <86box/mouse.h>
 #include <86box/config.h>
@@ -744,6 +746,66 @@ plat_pause(int p)
     }
 }
 
+void
+plat_init_rom_paths()
+{
+#ifndef __APPLE__
+    if (getenv("XDG_DATA_HOME")) {
+        char xdg_rom_path[1024] = { 0 };
+        strncpy(xdg_rom_path, getenv("XDG_DATA_HOME"), 1024);
+        plat_path_slash(xdg_rom_path);
+        strncat(xdg_rom_path, "86Box/", 1024);
+
+        if (!plat_dir_check(xdg_rom_path))
+            plat_dir_create(xdg_rom_path);
+        strcat(xdg_rom_path, "roms/");
+
+        if (!plat_dir_check(xdg_rom_path))
+            plat_dir_create(xdg_rom_path);
+        add_rom_path(xdg_rom_path);
+    } else {
+        char home_rom_path[1024] = { 0 };
+        snprintf(home_rom_path, 1024, "%s/.local/share/86Box/", getenv("HOME") ? getenv("HOME") : getpwuid(getuid())->pw_dir);
+
+        if (!plat_dir_check(home_rom_path))
+            plat_dir_create(home_rom_path);
+        strcat(home_rom_path, "roms/");
+
+        if (!plat_dir_check(home_rom_path))
+            plat_dir_create(home_rom_path);
+        add_rom_path(home_rom_path);
+    }
+    if (getenv("XDG_DATA_DIRS")) {
+        char* xdg_rom_paths = strdup(getenv("XDG_DATA_DIRS"));
+        char* xdg_rom_paths_orig = xdg_rom_paths;
+        char* cur_xdg_rom_path = NULL;
+        if (xdg_rom_paths) {
+            while (xdg_rom_paths[strlen(xdg_rom_paths) - 1] == ':') {
+                xdg_rom_paths[strlen(xdg_rom_paths) - 1] = '\0';
+            }
+            while ((cur_xdg_rom_path = local_strsep(&xdg_rom_paths, ";")) != NULL) {
+                char real_xdg_rom_path[1024] = { '\0' };
+                strcat(real_xdg_rom_path, cur_xdg_rom_path);
+                plat_path_slash(real_xdg_rom_path);
+                strcat(real_xdg_rom_path, "86Box/roms/");
+                add_rom_path(real_xdg_rom_path);
+            }
+        }
+        free(xdg_rom_paths_orig);
+    } else {
+        add_rom_path("/usr/local/share/86Box/roms/");
+        add_rom_path("/usr/share/86Box/roms/");
+    }
+#else
+    char home_rom_path[1024] = { '\0' };
+    snprintf(home_rom_path, 1024, "%s/Documents/86Box/", getenv("HOME") ? getenv("HOME") : getpwuid(getuid())->pw_dir);
+    plat_dir_create(home_rom_path);
+    strcat(home_rom_path, "roms/");
+    plat_dir_create(home_rom_path);
+    add_rom_path(home_rom_path);
+#endif
+}
+
 bool process_media_commands_3(uint8_t* id, char* fn, uint8_t* wp, int cmdargc)
 {
     bool err = false;
diff --git a/src/win/win.c b/src/win/win.c
index f4b906d7d..06db20bad 100644
--- a/src/win/win.c
+++ b/src/win/win.c
@@ -45,6 +45,8 @@
 #include <86box/timer.h>
 #include <86box/nvr.h>
 #include <86box/video.h>
+#include <86box/mem.h>
+#include <86box/rom.h>
 #define GLOBAL
 #include <86box/plat.h>
 #include <86box/ui.h>
@@ -910,6 +912,30 @@ plat_mmap(size_t size, uint8_t executable)
 }
 
 
+void
+plat_init_rom_paths()
+{
+    wchar_t appdata_dir[1024] = { L'\0' };
+
+    if (_wgetenv("LOCALAPPDATA") && _wgetenv("LOCALAPPDATA")[0] != L'\0') {
+        char appdata_dir_a[1024] = { '\0' };
+        size_t len = 0;
+        wcsncpy(appdata_dir, _wgetenv("LOCALAPPDATA"), 1024);
+        len = wcslen(appdata_dir);
+        if (appdata_dir[len - 1] != L'\\') {
+            appdata_dir[len] = L'\\';
+            appdata_dir[len + 1] = L'\0';
+        }
+        wcscat(appdata_dir, "86box");
+        CreateDirectoryW(appdata_dir, NULL);
+        wcscat(appdata_dir, "\\roms");
+        CreateDirectoryW(appdata_dir, NULL);
+        wcscat(appdata_dir, "\\");
+        c16stombs(appdata_dir_a, appdata_dir, 1024);
+        add_rom_path(appdata_dir_a);
+    }
+}
+
 void
 plat_munmap(void *ptr, size_t size)
 {